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Spontaneous object-location memory based on environmental geometry is impaired by both hippocampal and dorsolateral striatal lesions:

Spontaneous object-location memory based on environmental geometry is impaired by both... We examined the role of the hippocampus and the dorsolateral striatum in the representation of environmental geometry using a spontaneous object recognition procedure. Rats were placed in a kite-shaped arena and allowed to explore two distinctive objects in each of the right-angled corners. In a different room, rats were then placed into a rectangular arena with two identical copies of one of the two objects from the exploration phase, one in each of the two adjacent right-angled corners that were separated by a long wall. Time spent exploring these two objects was recorded as a measure of recognition memory. Since both objects were in different locations with respect to the room (different between exploration and test phases) and the global geometry (also different between exploration and test phases), differential exploration of the objects must be a result of initial habituation to the object relative to its local geometric context. The results indicated an impairment in processing the local geometric features of the environment for both hippocampus and dorsolateral striatum lesioned rats compared with sham-operated controls, though a control experiment showed these rats were unimpaired in a standard object recognition task. The dorsolateral striatum has previously been implicated in egocentric route-learning, but the results indicate an unexpected role for the dorsolateral striatum in processing the spatial layout of the environment. The results provide the first evidence that lesions to the hippocampus and dorsolateral striatum impair spontaneous encoding of local environmental geometric features. Keywords Spontaneous object recognition, context, geometry, cognitive map, hippocampus, dorsolateral striatum Received: 29 July 2020; accepted: 20 October 2020 non-random search at test indicates that animals did not rely Introduction solely on a global representation of space in the initial exposure The hippocampus (HPC) is often said to support a cognitive map to the training environment, but instead were guided by local spa- of the environment (O’Keefe and Nadel, 1978; Poulter et al., tial features that the two environments shared (McGregor et al., 2018) but what exactly is meant by a cognitive map is more 2006; Pearce et al., 2004; Tommasi and Polli, 2004). Pearce et al. equivocal (Bennett, 1996; Mackintosh, 2002). If a cognitive map (2004) and subsequently Jones et al. (2007) demonstrated that is a representation of the inter-relations among stimuli in the lesions to the HPC impaired navigation based on these local geo- environment (Leonard and McNaughton, 1990), an animal that metric properties of space. possessed one could represent the global layout of the environ- However, there is evidence of both global and local geometry ment. This notion is captured in the interpretation that when ani- controlling spatial behaviour in pigeons (Bingman et al., 2006), mals navigate relative to environmental geometry, they do so based on a configural representation of the shape of the environ- ment, abstracted from the elements creating it (Cheng and Spetch, Department of Psychology, Durham University, Durham, UK 1998; Gallistel, 1990). Department of Psychology, Waseda University, Tokyo, Japan To test whether animals form a representation of macroscopic geometric relations, animals trained in one environment are Corresponding author: tested in another, which shares some of its geometric features Anthony McGregor, Department of Psychology, Durham University, with that of the training environment. Crucially, the test environ- Durham DH1 3LE, UK. ment differs in its global shape to the training environment, so Email: anthony.mcgregor@durham.ac.uk Creative Commons CC BY: This article is distributed under the terms of the Creative Commons Attribution 4.0 License (https://creativecommons.org/licenses/by/4.0/) which permits any use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage). 2 Brain and Neuroscience Advances chicks (Kelly et al., 2011) and humans (Lew et al., 2014; Sturz certain the rat remained at the appropriate level of anaesthesia. et al., 2012). Sotelo et al. (2019), based on Pearce et al. (2004), An incision was made along the midline of the scalp and the trained pigeons to locate a reinforcer in one corner of a rectangu- bone covering the neocortex was removed using a dental burr. lar arena before transferring them to a kite shape, in which two An arm was mounted on to the stereotaxic frame to which was corners shared the same local geometric properties as the corners attached a 2-µL Hamilton syringe attached to an electronic micr- in the rectangle. Unlike Pearce et al. (2004), who found transfer odrive (model KDS 310; KD Scientific, New Hope, PA). The of rats’ search between environments, there was no evidence that microdrive controlled the quantity (0.05–0.25 µL) and rate pigeons recognised the matching local geometry between the two (0.03 µL/min) of excitotoxin. Ibotenic acid (Tocris Bioscience, arenas, despite learning the correct location within the rectangle. Bristol, UK), dissolved in phosphate-buffered saline (pH 7.4) to Furthermore, immediate early gene (IEG) analysis of hippocampal produce a 63 mM solution was infused in 28 and 12 injection c-Fos activation was higher for pigeons exposed to the familiar sites for each bilateral hippocampal and dorsolateral lesion, rectangle compared with others exposed to an unfamiliar trape- respectively. The infusion coordinates for the hippocampal zoid, suggesting that they recognised the overall shape of the lesions are reported in Coutureau et al. (1999) and the DLS rectangle but not of the trapezoid, and that this recognition was lesions in Kosaki et al. (2015). The needle was left in place for associated with hippocampal activity. 2 min following each infusion to permit diffusion of the ibotenic Therefore, the role of the HPC in learning based on local or acid into surrounding tissue. Sham-operated controls underwent global geometry remains uncertain. One difference between similar surgical procedures as for the HPC and DLS rats, with Pearce et al. (2004) and Sotelo et al. (2019), other than the species incision of the skin, neocortex exposed, and dura perforated tested, was the use of appetitive and aversive procedures, which using a needle, but no infusions were made. The incision was could have altered the way the animals behaved (Golob and sutured at the end of the procedure and the rat was placed into a Taube, 2002). To remove the confound of motivational reinforcer, warm chamber to recover. Each rat was administered subcuticu- we employed a spontaneous object recognition (SOR) version of lar Buprenorphine (0.01 mg/kg) pre- and post-procedure to pro- a geometry learning task (Experiment 1). We tested three groups vide analgesia, and a post-procedure subcuticular 10-mL saline – one with lesions to the HPC, a sham-operated control group, and and glucose solution to aid rehydration. Once sufficiently recov- one with lesions to the dorsolateral striatum (DLS). The DLS ered, the rat was transferred back to its home cage. A minimum group was included because there is little information on the of 14 days postoperative recovery was allowed before behav- effect of DLS lesions on object recognition. Korol et al. (2019) ioural testing began. recently examined the role of the DLS in SOR and found no evi- At the end of the experiment, rats were deeply anaesthetised dence for its involvement in object-location memory, so inclusion with sodium pentobarbitone (200 mg/kg) and perfused transcar- of this group acts as a positive control. However, Kosaki et al. dially with 0.9% saline followed by 4% paraformaldehyde solu- (2015) found that DLS lesions significantly facilitated place tion (0.1 M phosphate-buffered). Brains were removed and stored learning in a swimming pool, so one possibility was that we would in 4% paraformaldehyde solution (0.1 M phosphate-buffered) for see a similar facilitation in the current study. several days before being transferred to 25% sucrose (in 0.1 M phosphate-buffered saline) for 24–48 h before being sectioned (40 µm), mounted on slides, and stained with cresyl violet. Experiment 1 Apparatus. The apparatus was identical to that reported by Poul- Method ter et al. (2013). Briefly, a kite-shaped arena occupied one testing Subjects. The subjects were 32 male Lister hooded rats (Rattus room and a rectangular arena occupied another. The testing rooms norvegicus) supplied by Charles River (UK). They were approxi- had similar dimensions (approximately 290 × 185 × 260 cm mately 3 months of age when surgery was performed, and high) and each had a speaker mounted on the wall to provide 5 months old when testing on the current experiment was carried white noise, together with a table in the corner on which rats were out. They had been previously used in an unrelated water maze held. Each room was lit by a lamp that was placed on the floor task. The rats were housed in pairs in a light-proof, temperature- with an 11 W bulb and was positioned such that shadows were not controlled room (20°C), with the lights turned on at 07:00 h and cast into the arena. A camera was attached to a rail above each off at 21:00 h. Testing was conducted when the lights were turned arena, and images were transmitted to a monitor and recorder that on in the home room. All animals were provided with ad libitum were located in an adjacent room. The arenas were made from access to food and water. In total, 12 rats received lesions to the medium-density fibreboard and were painted light grey. Each HPC, 12 received lesions to the DLS, and 8 were sham-operated arena was made up of two long walls (100 × 50 cm high) and two controls. The experiment was conducted in accordance with the short walls (50 × 50 cm high). The walls in the kite were arranged Animals (Scientific Procedures) Act 1986 and Home Office and such that the corners where the long and short corners met were at institutional guidelines. an angle of 90°, so that they were geometrically identical to the corners in the rectangle (see Figure 2). The arenas were located on Surgical procedure. Each rat was deeply anaesthetised with a the floors of the testing rooms and could be rotated to occupy four mixture of isoflurane (5%) and oxygen (2 L/min), and its scalp different positions along a north-south or east-west axis. was shaved. It was then secured into a stereotaxic frame (Kopf Junk objects, including bottles, metal clips, ceramic orna- Instruments, Tujunga, CA, USA), with the incisor bar set at ments and small toys, occupied the corners of the arenas. Objects −3.3 mm. The anaesthetic was reduced to a maintenance concen- were chosen to be similar in terms of materials and dimensions tration (1%–2% isoflurane at 0.8 L/min), and the animal’s heart within a trial. They were affixed to the arena floor using Velcro. rate and reflexes were closely monitored throughout to make Multiple versions of the same objects were created so that Poulter et al. 3 different versions of the same object were presented in different the time a rat spent within a circular zone centred on each of the arenas during the sample and test phases. objects was recorded. There was a gap of approximately 5 cm between the edge of the object and the perimeter boundary of the zone. Thus, the time an animal spent within an area of 5 cm from Procedure. Rats were transported into the test laboratory, four at the object was recorded. To ensure tracking indexed exploration a time, in a holding cage comprising a Perspex bottom and wire only, time spent in the zone was only recorded if the rat’s head top. While transporting animals to and from the testing rooms, a entered either of these circular zones. This was automated by the fleece cover was placed over the cage to minimise the stress Ethovision software. It was also possible for the software to caused by this movement. Throughout behavioural procedures, record when the rat was not actively exploring, but instead the holding cage and rats, when not being tested, were placed on engaged in other activities, such as grooming. However, the a table in the corner of the room. Each trial commenced with the tracking system stopped tracking when contrast was lost between experimenter, always approaching the arena from the same the arena floor and the rat’s head, which occurred if the rat was southerly direction, placing the rat gently into the centre of the rearing. While we are confident that the automated tracking cap- arena. After the trial commenced, the experimenter left the test- tured active exploration, it may be that what we term ‘explora- ing room and waited in an adjacent room until the trial ended. On tion’ may include other behaviours. completion of the trial, the animal was removed from the arena and placed back into the holding cage. Rats received five sessions of habituation prior to beginning Statistical analysis. The time rats spent in the vicinity of each the experimental stage of the experiment. The first session of object was recorded for each of the four 120-s test phases. Mean habituation consisted of pairs of animals being placed into the time spent in the vicinity of each object over the four test phases rectangular arena, then into the kite, for 5 min in each. Sessions is reported. There was no minimum object exploration criterion two to five of habituation followed the same procedure as Session applied for each trial, but mean individual exploration across 1 with the exception that animals were now allowed to explore days varied between 15.3% and 33.1% of the test phase duration. each arena individually. Between each session of habituation, All data were analysed using two-way analysis of variance each arena was rotated 90° anticlockwise to ensure all rats (ANOVA). For Experiment 1, we predicted a group × object explored the empty arenas in each of the four possible orienta- interaction. Interactions were analysed using simple main effects tions. Each session of habituation took place on a separate day, analysis using the pooled error term from the original ANOVA. and animals were run in the same order throughout. The arenas were wiped down with dry paper towelling prior to each animal Results or pair of animals beginning exploration. At the end of each test- ing day, both arenas were cleaned with alcohol wipes. Figure 1 depicts reconstructions of the minimum (black shading) Following habituation, the experimental stage began, in which and maximum (grey shading) extent of hippocampal (A: left-hand animals received one object recognition trial per day for 4 days. In panel) and DLS (B: right-hand panel) lesions on a series of coronal the sample phase, each rat was exposed to two different objects, A sections. Rats in group HPC all sustained bilateral damage to the and B, in corners E and G of the kite, for 2 min (see Figure 2). dorsal and ventral HPC (CA fields 1–4), the dentate gyrus and the After a squad of four rats had completed the sample phase, they subicular cortices. The main sparing of hippocampal tissue was were then transported to the adjacent testing room for the test observed in the most medial areas of the dorsal HPC. One rat phase. In the test phase, which lasted for a further 2 min, each rat received lateral damage in both hemispheres that extended into the was placed in the rectangle arena in which two identical copies of lateral entorhinal and perirhinal cortices, so this animal was one of the objects were presented in the right-angled corners J and excluded from the analysis. In the majority of the remaining 11 K. The retention interval between the sample and test phase for rats, there was damage to the cortical area overlying the dorsal each rat was approximately 8 min. The orientation of the rectangle HPC. This typically included partial damage to motor, visual, changed between days but remained constant for all animals on somatosensory, parietal and retrosplenial agranular cortices (for the same day. Only two of the four possible kite orientations were reports of similar extrahippocampal damage in hippocamptomised used on any given day, although it was ensured that each orienta- rats, see Albasser et al., 2012; Iordanova et al., 2009). Similar to tion was counterbalanced equally between all animals. For the test Albasser et al. (2012), the partial cortical damage described above phase, animals were split into equal groups so that half received left plenty of sparing in each of these areas. For rats in group DLS, object A at test and the remainder object B, and, in so doing, visible widening of the lateral ventricles was observed in all cases ensured that the novel location (corner J or K of the rectangle) was owing to tissue shrinkage caused by the lesion. Inspection of the also assigned equally between animals. Thus, for each individual stained tissue revealed that the intended lesion site was off target in rat, the novel object-location corner changed daily. Therefore, any three rats. In these cases, which were excluded from subsequent preference for exploration of one object over another could not be analysis, there was significant extrastriatal damage to cortical areas explained by the positions of the objects with respect to generali- adjacent to the DLS. In the remaining rats, cell loss and modest sation between extramaze cues or by a preference for one right- gliosis was found in the targeted area. Thus, there were 11, 9 and 8 angled corner over another. On completion of a trial by an animal rats included in the behavioural analyses for group HPC, DLS and and prior to the next animal beginning their trial, each object was Sham, respectively. thoroughly cleaned with alcohol wipes and the arena was wiped To simplify the account of the behavioural results, it will be down with dry paper towelling. At the end of each testing day, assumed, as shown in the upper panel of Figure 2, that rats were both arenas were cleaned with alcohol wipes. exposed to objects A and B in corners E and G of the kite, before Ethovision (version 3.1) software was used to track the move- being presented with two copies of object A in corners J and K of ment of each animal in the test phase. For each 120-s test phase, the rectangle. In fact, however, the locations of objects A and B 4 Brain and Neuroscience Advances Figure 1. Coronal sections displaying the extent of (a) hippocampal damage and (b) DLS damage. The case with the largest (grey shading) and smallest (black shading) amount of tissue loss is represented for each lesion group. The numbers refer to the distance anterior or posterior to bregma for each section, according to Paxinos and Watson (2007). in the sample phase and the identity of the object (A or B) at test appeared to discriminate locations. A two-way ANOVA of mean were counterbalanced. With reference to Figure 2, corner E of the object exploration times over the four test trials, with group kite is the geometric equivalent of corner K in the rectangle (Sham, HPC and DLS) and object location (novel, familiar) as factors, failed to reveal a significant group × object location because in both corners, the long wall is to the left of a short wall. interaction, F(2, 25) = 3.36, p = 0.051, but as there was an a priori Thus, it was expected that object A in corner J of the rectangle prediction that the groups would differ, planned comparisons would be explored more than object A in corner K, as it was in a were used to examine group differences. Analysis of simple main novel location relative to the local geometric cues provided by effects using the pooled error term revealed that group Sham the arena, whereas object A in corner J was in a familiar spent more time near the object in the novel than the familiar location. location, F(1, 25) = 4.44, p = 0.045, but that groups HPC, F(1, The mean times that rats in each group spent in the vicinity of 25) = 2.06, p = 0.16, and DLS, F(1, 25) = 0.21, p = 0.65, did not. objects in the novel and familiar locations in the test phase are These differences are illustrated more clearly in the lower panel shown in the lower panel of Figure 2. Overall, exploration was of Figure 2, which shows group means for time spent near the similar between groups, but the Sham group appeared to spend object in the novel and familiar location, along with the 95% con- more time in the vicinity of the object in the novel location com- fidence interval for the mean difference between the exploration pared with the familiar location. Neither the HPC or DLS groups Poulter et al. 5 Figure 2. The upper panel shows a schematic diagram showing the design of Experiment 1. The arenas were in different experimental Figure 3. The upper panel shows a schematic diagram showing the rooms. Objects A and B are represented by circular and square symbols, design of Experiment 2. The two arenas were housed in different respectively. Preferential exploration of object A in corner J of the rooms. Objects A and B are represented by circular and square symbols, rectangle over the identical object in corner K indicates the animal’s respectively. Preferential exploration of object B over object A detection of its novel location, despite the fact both of the objects indicates the animal’s detection of its novelty. The positions of objects were placed in a differently shaped arena in a different room. The lower A and B varied over trials and between rats so the positions of the panel shows the mean exploration times of each of the two test objects objects relative to the local geometric features of the rectangle were for each of the three groups. The error bars show the 95% confidence irrelevant for successful performance. The lower panel shows the mean interval for the mean within-group difference between exploration exploration times of each of the two test objects for each of the three times for the two objects, based on the pooled error term. groups. The error bars show the 95% confidence interval for the mean within-group difference between exploration times for the two objects, based on the pooled error term. times, shown arbitrarily on the novel object mean bar. The main effects of object location, F(1, 25) = 0.08, p = 0.79, and group, F(2, 25) = 1.83, p = 0.18, were not significant. followed by objects A and B in corners J and K of the rectangle. The results indicate an impairment for both HPC and DLS In essence, this procedure emulates a standard object recognition groups, compared with group Sham. Before discussing the results procedure, but with the equivalent changes in global and local further, we report Experiment 2, designed as a control to ensure context that were encountered by rats in Experiment 1. A sche- that the lesions did not impair discrimination based on a non- matic representation of the design of Experiment 2 is shown in spatial version of the procedure. the upper panel of Figure 3. Results Experiment 2 The mean times spent in the vicinity of the novel and familiar Method objects by each group in the test phase are shown in the lower The subjects and apparatus were identical to Experiment 1. The panel of Figure 3. A two-way ANOVA of mean exploration procedure was identical to Experiment 1 with the following times over the four test trials, with group and object as factors, exceptions. First, instead of undergoing the same habituation showed significant main effects of object, F(1, 25) = 22.98, phase as in Experiment 1, rats were given a single refresher habit- p < 0.001. Post hoc pairwise comparisons showed that each uation session, which involved them spending 5 min in their group discriminated the novel from the familiar object, ps < 0.05. holding case in each testing room. Second, for the experimental There was also a main effect of group, F(2, 25) = 14.31, stage, instead of being presented with two different objects in the p < 0.001, but no object × lesion interaction, F(2, 25) = 0.24, right-angled corners of the kite, in Experiment 2, rats were pre- p = 0.79. For the main effect of group, pairwise comparisons sented with two copies of object A in corners E and G of the kite, showed that group HPC spent more time exploring objects 6 Brain and Neuroscience Advances have caused differences in the results that are not due purely to overall than groups Sham and DLS, ps < 0.001, though groups the effects of the lesions on the representation of geometry. Sham and DLS did not differ, p > 0.5. However, had the lesions produced a systematic change to the way the lesion groups explored objects, we would have expected a difference between the groups in Experiment 2 as well, which Discussion served as a control condition. In addition, a number of other stud- Several rodent studies have shown that the HPC is necessary for ies (e.g. Ennaceur et al., 1997; Mumby et al., 2002) suggest that SOR in which an animal must integrate object identity with spa- lesions to the HPC do not affect exploration of objects in the tial (Aggleton and Nelson, 2020; Bussey et al., 2000; Good et al., sample phase of a SOR task. Also, Gaskin et al. (2010) show that 2007; Save et al., 1992), featural (Good et al., 2007; Mumby sample exploration does not predict test phase performance in et al., 2002) or temporal (Good et al., 2007) information. SOR tasks. Conversely, numerous studies have demonstrated that rodents One of the reasons for conducting our study was the conflict- with hippocampal lesions are not impaired in standard object rec- ing evidence over the role of the HPC in representing environ- ognition (Ainge et al., 2006; Mumby et al., 2002). The results of mental geometry. While experiments with rats seemed to indicate Experiment 1 add to the body of evidence implicating the HPC in that the HPC was necessary for representing local geometric fea- object-location memory, while extending our knowledge of how tures, such as the configuration of long and short walls in a par- location is represented. The results of Experiment 2 confirmed ticular corner (e.g. Jones et al., 2007; McGregor et al., 2004; that the lesions did not affect standard object recognition mem- Pearce et al., 2004), recent research in pigeons (Sotelo et al., ory, while equating some of the procedural and contextual 2019) casts doubt on this conclusion because pigeons showed no changes encountered by rats in Experiment 1. transfer between environments based on local geometry, but hip- As predicted, group Sham discriminated locations with refer- pocampal c-Fos analysis indicated hippocampal activity when ence to the local geometric context in which an object was first pigeons experienced transfer to a familiar overall shape. encountered. The result replicates the findings of Poulter et al. Importantly, the SOR procedure used in our experiments removes (2013), though it should be noted that the current study had a the confound of the nature of the motivational demands of the substantially smaller sample size, so statistical power was procedure since the pigeon study used an appetitive procedure, weaker. One way to ensure that the results in the current study while the rat studies used an aversive motivation. The SOR pro- replicated those of Poulter et al. (2013) is to calculate the replica- cedure also removes the possibility that the previously reported tion Bayes factor (BF), as described by Ly et al. (2019). The effects of HPC lesions on learning based on local geometry were Sham group in Experiment 1 is a direct replication of Poulter because of disruption to the formation of stimulus-response hab- et al.’s (2013) Experiment 2. Therefore, taking a single measure its in the swimming pool, which were reported by Jones et al. of discrimination, the d2 score (novel − familiar/novel + famil- (2007). Our finding that lesions to the HPC disrupted the use of iar), from both Poulter et al.’s (2013) study and the sham data local geometric context for object location in an untrained, nona- from the current study, we calculated the replication BF . This versive procedure provides renewed evidence for the role of the was done by calculating the BF of the combined original and HPC in learning based on local geometry (Pearce et al., 2004). It current d2 scores, compared to a chance level of zero. Following also corresponds with recent evidence from the electrophysiolog- Ly et al. (2019), this combined BF , BF = 17.586, was divided ical literature that changing environmental geometry alters the 10 10 by the BF of the original d2 scores, also compared to chance, local firing patterns of entorhinal grid cells, which are part of the BF = 5.759. The result, BF = 3.05, is the replication BF and hippocampal cognitive mapping system, but that more distant 10 10 10 indicates that the sham data provide evidence for replication grid fields are unaffected by changes to environmental geometry three times greater (precisely, 3.05 times greater) than for the (Krupic et al., 2018). alternative of no replication. We are therefore confident that the However, our results also raise the question of why Sotelo sham results reflect a genuine effect. et al. (2019) were unable to replicate Pearce et al.’s (2004) find- In terms of recognition memory for object location, the results ings, but still found c-Fos activation in the HPC. In terms of the are important in understanding the cues necessary to define a spa- use of local geometry, the use of an appetitive task may have had tial location in recognition memory. In previous object-location an effect. Golob and Taube (2002) reported rats relying more on recognition memory procedures, the location of a familiar object a non-geometric landmark than on environmental geometry is often swapped with that of another or simply displaced (e.g. when motivated by escape from water than when motivated by a Dix and Aggleton, 1999; Good et al., 2007), meaning that both food reinforcer: Cheng’s (1986) original finding that rats prefer- the relative positions of the objects, with reference to other entially relied on geometry over non-geometric features was also objects in the array, and the absolute positions of the objects, with based on an appetitive task (but see Lee et al., 2020 for evidence reference to room cues, could be used to define spatial location that rats in an appetitive reorientation task also coded the non- (see also Langston and Wood, 2010; Wilson et al., 2013, for evi- geometric features of the environment). The differential effect of dence that egocentric strategies may underlie some object-loca- motivation has been also observed in the use of spatial strategies: tion memory). Our results demonstrate that the local geometric Asem and Holland (2013) showed that rats in a water-submerged context in which the object was encountered is sufficient for plus-maze relied on an egocentric response strategy early in object-location recognition memory since both the absolute and training, switching to an allocentric place strategy later, but found relative positions of the objects changed between the exploration the opposite pattern of results when the maze was drained and the and test phases. It should be noted that we did not record explora- escape platform replaced by the opportunity to find food. Turning tion of objects during the sample phase. It might be argued that to Sotelo et al.’s (2019) report of hippocampal c-Fos activation differential group exploration during the sample phase might when pigeons encountered transfer from a rectangle to another Poulter et al. 7 rectangle, but no activation when they transferred from a rectan- an egocentric representation. For example, the position of object gle to a trapezoid, we are only in a position to speculate a reason. A in the kite may have been encoded by remembering that it was One argument is that our lesion study provides stronger evidence to the rat’s left in one right-angled corner, relative to a salient of a causal link between the HPC and object-location memory feature, such as the end of a long wall, while object B was than the correlational nature of IEG activation (Sotelo et al., remembered to the rat’s right in the right-angled corner, relative 2019), though Bingman et al. (2006) showed that hippocampal to the end of the long wall. At test, the unexpected position of lesions impaired pigeons’ reliance on geometric cues. Another object A to the rat’s right at the end of the long wall would have possibility is that there was a discrepancy between the sensitivity caused dishabituation and renewed exploration, but only if the rat of the behavioural task and that of the neural activation, meaning was capable of such an egocentric representation. A number of it was easier to detect changes to IEG expression than it was for possible permutations for this kind of egocentric encoding are behaviour. The possibility also remains that there is a fundamen- possible, but if this is the case then successful object-location tal difference between species in their local and global represen- memory may depend not only on disambiguating long and short tations of space. This possibility seems less likely, however, in walls, involving the HPC, but also coding the object locations light of Tommasi and Polli’s (2004) conclusion that chicks repre- with reference to the positions of long and short walls relative to sent local geometric features rather than global geometry. the rats’ own bodies. To our knowledge, only Korol et al. (2019) Nevertheless, Sotelo et al. (2020) have recently found that the have explored the role of the DLS in a SOR procedure. They terrestrial toad, Rhinella arenarum, also fails to transfer between reported that inactivation of the DLS impaired rats’ memory for a rectangle and kite, and Sotelo et al. (2016) showed that c-Fos the identities of previously encountered objects, but not their activation in the medial pallium of the same species, a putative locations. However, their object-location procedure involved homologue of the mammalian HPC, increased as a result of shifting the positions of two previously encountered objects from exposure to environmental geometry. The possibility of between 40 cm apart to 10 cm apart in an otherwise featureless plexiglass species differences therefore remains. This possibility is made arena. Because objects in our experiment shifted in absolute and greater by the finding that humans are able to use both local and relative positions, only the local geometric context could be used global representations of space (e.g. Buckley et al., 2016, 2019a, to disambiguate objects, which is considerably different from 2019b; Lew et al., 2014; Sturz et al., 2012, 2018), though it Korol et al.’s procedure. should be noted that the role of the HPC in these representations While our results with DLS lesions are novel, their interpreta- has not been investigated. tion does require some speculation which requires further In terms of understanding the nature of the impairments to research. Nevertheless, the results of our experiments provide both the HPC and DLS groups in Experiment 1, it is necessary to further evidence that animals represent the local geometric fea- consider how normal rats represented local geometry. Jones et al. tures of their environment, and that this encoding is automatic, (2007) showed that lesions to the HPC impaired rats’ ability to being evident from recognition memory. This local representa- use the direct metric information provided by wall length. Our tion is impaired by lesions to the HPC, which provides further results for the HPC group are consistent with this finding and support for the argument that HPC-dependent cognitive maps of suggest that sham animals retained their ability to represent the the environment are based on local representations of space. different lengths of walls in the two environments. However, unlike in Jones et al. (2007) our use of an untrained procedure Declaration of conflicting interests prevented sham animals from developing turning habits that The author(s) declared no potential conflicts of interest with respect to seemed to underlie at least some level of successful performance the research, authorship, and/or publication of this article. during training. In Experiment 2, there was no impairment in a standard object recognition task, albeit adapted to control for the Funding context change encountered by rats in Experiment 1. Relevant to the results of Experiment 2, O’Brien et al. (2006) and Piterkin The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was et al. (2008) found that HPC lesions impaired the ability of rats to supported by Biotechnology and Biological Sciences Research Council recognise previously encountered objects when the test context grants to D.J.S. and A.M. (Nos BB/M009440/1 and BB/F013094/1) was different from the sample context, which we did not find. In light of these findings, our hypothesis about rats coding the local rather than the global geometric properties of the environment is ORCID iD lent more weight as our HPC rats seemed not to detect the change Anthony McGregor https://orcid.org/0000-0003-0265-828X in context, as would be expected if they only coded the local features of corners in which objects were encountered, which References were the same across the exploration and test phases. Turning to the results for the DLS group, we included this Aggleton JP and Nelson AJD (2020) Distributed interactive brain cir- cuits for object-in-place memory: A place for time? Brain and group as a positive control since lesions or inactivation of the Neuroscience Advances 4. Epub ahead of print 30 June. 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Wilson DIG, Langston RF, Schlesiger MI, et al. (2013) Lateral entorhinal Sturz BR, Bell ZK and Bodily KD (2018) Environmental scaling influ- cortex is critical for novel object-context recognition. Hippocampus ences the use of local but not global geometric cues during spatial 23(5): 352–366. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Brain and Neuroscience Advances SAGE

Spontaneous object-location memory based on environmental geometry is impaired by both hippocampal and dorsolateral striatal lesions:

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Abstract

We examined the role of the hippocampus and the dorsolateral striatum in the representation of environmental geometry using a spontaneous object recognition procedure. Rats were placed in a kite-shaped arena and allowed to explore two distinctive objects in each of the right-angled corners. In a different room, rats were then placed into a rectangular arena with two identical copies of one of the two objects from the exploration phase, one in each of the two adjacent right-angled corners that were separated by a long wall. Time spent exploring these two objects was recorded as a measure of recognition memory. Since both objects were in different locations with respect to the room (different between exploration and test phases) and the global geometry (also different between exploration and test phases), differential exploration of the objects must be a result of initial habituation to the object relative to its local geometric context. The results indicated an impairment in processing the local geometric features of the environment for both hippocampus and dorsolateral striatum lesioned rats compared with sham-operated controls, though a control experiment showed these rats were unimpaired in a standard object recognition task. The dorsolateral striatum has previously been implicated in egocentric route-learning, but the results indicate an unexpected role for the dorsolateral striatum in processing the spatial layout of the environment. The results provide the first evidence that lesions to the hippocampus and dorsolateral striatum impair spontaneous encoding of local environmental geometric features. Keywords Spontaneous object recognition, context, geometry, cognitive map, hippocampus, dorsolateral striatum Received: 29 July 2020; accepted: 20 October 2020 non-random search at test indicates that animals did not rely Introduction solely on a global representation of space in the initial exposure The hippocampus (HPC) is often said to support a cognitive map to the training environment, but instead were guided by local spa- of the environment (O’Keefe and Nadel, 1978; Poulter et al., tial features that the two environments shared (McGregor et al., 2018) but what exactly is meant by a cognitive map is more 2006; Pearce et al., 2004; Tommasi and Polli, 2004). Pearce et al. equivocal (Bennett, 1996; Mackintosh, 2002). If a cognitive map (2004) and subsequently Jones et al. (2007) demonstrated that is a representation of the inter-relations among stimuli in the lesions to the HPC impaired navigation based on these local geo- environment (Leonard and McNaughton, 1990), an animal that metric properties of space. possessed one could represent the global layout of the environ- However, there is evidence of both global and local geometry ment. This notion is captured in the interpretation that when ani- controlling spatial behaviour in pigeons (Bingman et al., 2006), mals navigate relative to environmental geometry, they do so based on a configural representation of the shape of the environ- ment, abstracted from the elements creating it (Cheng and Spetch, Department of Psychology, Durham University, Durham, UK 1998; Gallistel, 1990). Department of Psychology, Waseda University, Tokyo, Japan To test whether animals form a representation of macroscopic geometric relations, animals trained in one environment are Corresponding author: tested in another, which shares some of its geometric features Anthony McGregor, Department of Psychology, Durham University, with that of the training environment. Crucially, the test environ- Durham DH1 3LE, UK. ment differs in its global shape to the training environment, so Email: anthony.mcgregor@durham.ac.uk Creative Commons CC BY: This article is distributed under the terms of the Creative Commons Attribution 4.0 License (https://creativecommons.org/licenses/by/4.0/) which permits any use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage). 2 Brain and Neuroscience Advances chicks (Kelly et al., 2011) and humans (Lew et al., 2014; Sturz certain the rat remained at the appropriate level of anaesthesia. et al., 2012). Sotelo et al. (2019), based on Pearce et al. (2004), An incision was made along the midline of the scalp and the trained pigeons to locate a reinforcer in one corner of a rectangu- bone covering the neocortex was removed using a dental burr. lar arena before transferring them to a kite shape, in which two An arm was mounted on to the stereotaxic frame to which was corners shared the same local geometric properties as the corners attached a 2-µL Hamilton syringe attached to an electronic micr- in the rectangle. Unlike Pearce et al. (2004), who found transfer odrive (model KDS 310; KD Scientific, New Hope, PA). The of rats’ search between environments, there was no evidence that microdrive controlled the quantity (0.05–0.25 µL) and rate pigeons recognised the matching local geometry between the two (0.03 µL/min) of excitotoxin. Ibotenic acid (Tocris Bioscience, arenas, despite learning the correct location within the rectangle. Bristol, UK), dissolved in phosphate-buffered saline (pH 7.4) to Furthermore, immediate early gene (IEG) analysis of hippocampal produce a 63 mM solution was infused in 28 and 12 injection c-Fos activation was higher for pigeons exposed to the familiar sites for each bilateral hippocampal and dorsolateral lesion, rectangle compared with others exposed to an unfamiliar trape- respectively. The infusion coordinates for the hippocampal zoid, suggesting that they recognised the overall shape of the lesions are reported in Coutureau et al. (1999) and the DLS rectangle but not of the trapezoid, and that this recognition was lesions in Kosaki et al. (2015). The needle was left in place for associated with hippocampal activity. 2 min following each infusion to permit diffusion of the ibotenic Therefore, the role of the HPC in learning based on local or acid into surrounding tissue. Sham-operated controls underwent global geometry remains uncertain. One difference between similar surgical procedures as for the HPC and DLS rats, with Pearce et al. (2004) and Sotelo et al. (2019), other than the species incision of the skin, neocortex exposed, and dura perforated tested, was the use of appetitive and aversive procedures, which using a needle, but no infusions were made. The incision was could have altered the way the animals behaved (Golob and sutured at the end of the procedure and the rat was placed into a Taube, 2002). To remove the confound of motivational reinforcer, warm chamber to recover. Each rat was administered subcuticu- we employed a spontaneous object recognition (SOR) version of lar Buprenorphine (0.01 mg/kg) pre- and post-procedure to pro- a geometry learning task (Experiment 1). We tested three groups vide analgesia, and a post-procedure subcuticular 10-mL saline – one with lesions to the HPC, a sham-operated control group, and and glucose solution to aid rehydration. Once sufficiently recov- one with lesions to the dorsolateral striatum (DLS). The DLS ered, the rat was transferred back to its home cage. A minimum group was included because there is little information on the of 14 days postoperative recovery was allowed before behav- effect of DLS lesions on object recognition. Korol et al. (2019) ioural testing began. recently examined the role of the DLS in SOR and found no evi- At the end of the experiment, rats were deeply anaesthetised dence for its involvement in object-location memory, so inclusion with sodium pentobarbitone (200 mg/kg) and perfused transcar- of this group acts as a positive control. However, Kosaki et al. dially with 0.9% saline followed by 4% paraformaldehyde solu- (2015) found that DLS lesions significantly facilitated place tion (0.1 M phosphate-buffered). Brains were removed and stored learning in a swimming pool, so one possibility was that we would in 4% paraformaldehyde solution (0.1 M phosphate-buffered) for see a similar facilitation in the current study. several days before being transferred to 25% sucrose (in 0.1 M phosphate-buffered saline) for 24–48 h before being sectioned (40 µm), mounted on slides, and stained with cresyl violet. Experiment 1 Apparatus. The apparatus was identical to that reported by Poul- Method ter et al. (2013). Briefly, a kite-shaped arena occupied one testing Subjects. The subjects were 32 male Lister hooded rats (Rattus room and a rectangular arena occupied another. The testing rooms norvegicus) supplied by Charles River (UK). They were approxi- had similar dimensions (approximately 290 × 185 × 260 cm mately 3 months of age when surgery was performed, and high) and each had a speaker mounted on the wall to provide 5 months old when testing on the current experiment was carried white noise, together with a table in the corner on which rats were out. They had been previously used in an unrelated water maze held. Each room was lit by a lamp that was placed on the floor task. The rats were housed in pairs in a light-proof, temperature- with an 11 W bulb and was positioned such that shadows were not controlled room (20°C), with the lights turned on at 07:00 h and cast into the arena. A camera was attached to a rail above each off at 21:00 h. Testing was conducted when the lights were turned arena, and images were transmitted to a monitor and recorder that on in the home room. All animals were provided with ad libitum were located in an adjacent room. The arenas were made from access to food and water. In total, 12 rats received lesions to the medium-density fibreboard and were painted light grey. Each HPC, 12 received lesions to the DLS, and 8 were sham-operated arena was made up of two long walls (100 × 50 cm high) and two controls. The experiment was conducted in accordance with the short walls (50 × 50 cm high). The walls in the kite were arranged Animals (Scientific Procedures) Act 1986 and Home Office and such that the corners where the long and short corners met were at institutional guidelines. an angle of 90°, so that they were geometrically identical to the corners in the rectangle (see Figure 2). The arenas were located on Surgical procedure. Each rat was deeply anaesthetised with a the floors of the testing rooms and could be rotated to occupy four mixture of isoflurane (5%) and oxygen (2 L/min), and its scalp different positions along a north-south or east-west axis. was shaved. It was then secured into a stereotaxic frame (Kopf Junk objects, including bottles, metal clips, ceramic orna- Instruments, Tujunga, CA, USA), with the incisor bar set at ments and small toys, occupied the corners of the arenas. Objects −3.3 mm. The anaesthetic was reduced to a maintenance concen- were chosen to be similar in terms of materials and dimensions tration (1%–2% isoflurane at 0.8 L/min), and the animal’s heart within a trial. They were affixed to the arena floor using Velcro. rate and reflexes were closely monitored throughout to make Multiple versions of the same objects were created so that Poulter et al. 3 different versions of the same object were presented in different the time a rat spent within a circular zone centred on each of the arenas during the sample and test phases. objects was recorded. There was a gap of approximately 5 cm between the edge of the object and the perimeter boundary of the zone. Thus, the time an animal spent within an area of 5 cm from Procedure. Rats were transported into the test laboratory, four at the object was recorded. To ensure tracking indexed exploration a time, in a holding cage comprising a Perspex bottom and wire only, time spent in the zone was only recorded if the rat’s head top. While transporting animals to and from the testing rooms, a entered either of these circular zones. This was automated by the fleece cover was placed over the cage to minimise the stress Ethovision software. It was also possible for the software to caused by this movement. Throughout behavioural procedures, record when the rat was not actively exploring, but instead the holding cage and rats, when not being tested, were placed on engaged in other activities, such as grooming. However, the a table in the corner of the room. Each trial commenced with the tracking system stopped tracking when contrast was lost between experimenter, always approaching the arena from the same the arena floor and the rat’s head, which occurred if the rat was southerly direction, placing the rat gently into the centre of the rearing. While we are confident that the automated tracking cap- arena. After the trial commenced, the experimenter left the test- tured active exploration, it may be that what we term ‘explora- ing room and waited in an adjacent room until the trial ended. On tion’ may include other behaviours. completion of the trial, the animal was removed from the arena and placed back into the holding cage. Rats received five sessions of habituation prior to beginning Statistical analysis. The time rats spent in the vicinity of each the experimental stage of the experiment. The first session of object was recorded for each of the four 120-s test phases. Mean habituation consisted of pairs of animals being placed into the time spent in the vicinity of each object over the four test phases rectangular arena, then into the kite, for 5 min in each. Sessions is reported. There was no minimum object exploration criterion two to five of habituation followed the same procedure as Session applied for each trial, but mean individual exploration across 1 with the exception that animals were now allowed to explore days varied between 15.3% and 33.1% of the test phase duration. each arena individually. Between each session of habituation, All data were analysed using two-way analysis of variance each arena was rotated 90° anticlockwise to ensure all rats (ANOVA). For Experiment 1, we predicted a group × object explored the empty arenas in each of the four possible orienta- interaction. Interactions were analysed using simple main effects tions. Each session of habituation took place on a separate day, analysis using the pooled error term from the original ANOVA. and animals were run in the same order throughout. The arenas were wiped down with dry paper towelling prior to each animal Results or pair of animals beginning exploration. At the end of each test- ing day, both arenas were cleaned with alcohol wipes. Figure 1 depicts reconstructions of the minimum (black shading) Following habituation, the experimental stage began, in which and maximum (grey shading) extent of hippocampal (A: left-hand animals received one object recognition trial per day for 4 days. In panel) and DLS (B: right-hand panel) lesions on a series of coronal the sample phase, each rat was exposed to two different objects, A sections. Rats in group HPC all sustained bilateral damage to the and B, in corners E and G of the kite, for 2 min (see Figure 2). dorsal and ventral HPC (CA fields 1–4), the dentate gyrus and the After a squad of four rats had completed the sample phase, they subicular cortices. The main sparing of hippocampal tissue was were then transported to the adjacent testing room for the test observed in the most medial areas of the dorsal HPC. One rat phase. In the test phase, which lasted for a further 2 min, each rat received lateral damage in both hemispheres that extended into the was placed in the rectangle arena in which two identical copies of lateral entorhinal and perirhinal cortices, so this animal was one of the objects were presented in the right-angled corners J and excluded from the analysis. In the majority of the remaining 11 K. The retention interval between the sample and test phase for rats, there was damage to the cortical area overlying the dorsal each rat was approximately 8 min. The orientation of the rectangle HPC. This typically included partial damage to motor, visual, changed between days but remained constant for all animals on somatosensory, parietal and retrosplenial agranular cortices (for the same day. Only two of the four possible kite orientations were reports of similar extrahippocampal damage in hippocamptomised used on any given day, although it was ensured that each orienta- rats, see Albasser et al., 2012; Iordanova et al., 2009). Similar to tion was counterbalanced equally between all animals. For the test Albasser et al. (2012), the partial cortical damage described above phase, animals were split into equal groups so that half received left plenty of sparing in each of these areas. For rats in group DLS, object A at test and the remainder object B, and, in so doing, visible widening of the lateral ventricles was observed in all cases ensured that the novel location (corner J or K of the rectangle) was owing to tissue shrinkage caused by the lesion. Inspection of the also assigned equally between animals. Thus, for each individual stained tissue revealed that the intended lesion site was off target in rat, the novel object-location corner changed daily. Therefore, any three rats. In these cases, which were excluded from subsequent preference for exploration of one object over another could not be analysis, there was significant extrastriatal damage to cortical areas explained by the positions of the objects with respect to generali- adjacent to the DLS. In the remaining rats, cell loss and modest sation between extramaze cues or by a preference for one right- gliosis was found in the targeted area. Thus, there were 11, 9 and 8 angled corner over another. On completion of a trial by an animal rats included in the behavioural analyses for group HPC, DLS and and prior to the next animal beginning their trial, each object was Sham, respectively. thoroughly cleaned with alcohol wipes and the arena was wiped To simplify the account of the behavioural results, it will be down with dry paper towelling. At the end of each testing day, assumed, as shown in the upper panel of Figure 2, that rats were both arenas were cleaned with alcohol wipes. exposed to objects A and B in corners E and G of the kite, before Ethovision (version 3.1) software was used to track the move- being presented with two copies of object A in corners J and K of ment of each animal in the test phase. For each 120-s test phase, the rectangle. In fact, however, the locations of objects A and B 4 Brain and Neuroscience Advances Figure 1. Coronal sections displaying the extent of (a) hippocampal damage and (b) DLS damage. The case with the largest (grey shading) and smallest (black shading) amount of tissue loss is represented for each lesion group. The numbers refer to the distance anterior or posterior to bregma for each section, according to Paxinos and Watson (2007). in the sample phase and the identity of the object (A or B) at test appeared to discriminate locations. A two-way ANOVA of mean were counterbalanced. With reference to Figure 2, corner E of the object exploration times over the four test trials, with group kite is the geometric equivalent of corner K in the rectangle (Sham, HPC and DLS) and object location (novel, familiar) as factors, failed to reveal a significant group × object location because in both corners, the long wall is to the left of a short wall. interaction, F(2, 25) = 3.36, p = 0.051, but as there was an a priori Thus, it was expected that object A in corner J of the rectangle prediction that the groups would differ, planned comparisons would be explored more than object A in corner K, as it was in a were used to examine group differences. Analysis of simple main novel location relative to the local geometric cues provided by effects using the pooled error term revealed that group Sham the arena, whereas object A in corner J was in a familiar spent more time near the object in the novel than the familiar location. location, F(1, 25) = 4.44, p = 0.045, but that groups HPC, F(1, The mean times that rats in each group spent in the vicinity of 25) = 2.06, p = 0.16, and DLS, F(1, 25) = 0.21, p = 0.65, did not. objects in the novel and familiar locations in the test phase are These differences are illustrated more clearly in the lower panel shown in the lower panel of Figure 2. Overall, exploration was of Figure 2, which shows group means for time spent near the similar between groups, but the Sham group appeared to spend object in the novel and familiar location, along with the 95% con- more time in the vicinity of the object in the novel location com- fidence interval for the mean difference between the exploration pared with the familiar location. Neither the HPC or DLS groups Poulter et al. 5 Figure 2. The upper panel shows a schematic diagram showing the design of Experiment 1. The arenas were in different experimental Figure 3. The upper panel shows a schematic diagram showing the rooms. Objects A and B are represented by circular and square symbols, design of Experiment 2. The two arenas were housed in different respectively. Preferential exploration of object A in corner J of the rooms. Objects A and B are represented by circular and square symbols, rectangle over the identical object in corner K indicates the animal’s respectively. Preferential exploration of object B over object A detection of its novel location, despite the fact both of the objects indicates the animal’s detection of its novelty. The positions of objects were placed in a differently shaped arena in a different room. The lower A and B varied over trials and between rats so the positions of the panel shows the mean exploration times of each of the two test objects objects relative to the local geometric features of the rectangle were for each of the three groups. The error bars show the 95% confidence irrelevant for successful performance. The lower panel shows the mean interval for the mean within-group difference between exploration exploration times of each of the two test objects for each of the three times for the two objects, based on the pooled error term. groups. The error bars show the 95% confidence interval for the mean within-group difference between exploration times for the two objects, based on the pooled error term. times, shown arbitrarily on the novel object mean bar. The main effects of object location, F(1, 25) = 0.08, p = 0.79, and group, F(2, 25) = 1.83, p = 0.18, were not significant. followed by objects A and B in corners J and K of the rectangle. The results indicate an impairment for both HPC and DLS In essence, this procedure emulates a standard object recognition groups, compared with group Sham. Before discussing the results procedure, but with the equivalent changes in global and local further, we report Experiment 2, designed as a control to ensure context that were encountered by rats in Experiment 1. A sche- that the lesions did not impair discrimination based on a non- matic representation of the design of Experiment 2 is shown in spatial version of the procedure. the upper panel of Figure 3. Results Experiment 2 The mean times spent in the vicinity of the novel and familiar Method objects by each group in the test phase are shown in the lower The subjects and apparatus were identical to Experiment 1. The panel of Figure 3. A two-way ANOVA of mean exploration procedure was identical to Experiment 1 with the following times over the four test trials, with group and object as factors, exceptions. First, instead of undergoing the same habituation showed significant main effects of object, F(1, 25) = 22.98, phase as in Experiment 1, rats were given a single refresher habit- p < 0.001. Post hoc pairwise comparisons showed that each uation session, which involved them spending 5 min in their group discriminated the novel from the familiar object, ps < 0.05. holding case in each testing room. Second, for the experimental There was also a main effect of group, F(2, 25) = 14.31, stage, instead of being presented with two different objects in the p < 0.001, but no object × lesion interaction, F(2, 25) = 0.24, right-angled corners of the kite, in Experiment 2, rats were pre- p = 0.79. For the main effect of group, pairwise comparisons sented with two copies of object A in corners E and G of the kite, showed that group HPC spent more time exploring objects 6 Brain and Neuroscience Advances have caused differences in the results that are not due purely to overall than groups Sham and DLS, ps < 0.001, though groups the effects of the lesions on the representation of geometry. Sham and DLS did not differ, p > 0.5. However, had the lesions produced a systematic change to the way the lesion groups explored objects, we would have expected a difference between the groups in Experiment 2 as well, which Discussion served as a control condition. In addition, a number of other stud- Several rodent studies have shown that the HPC is necessary for ies (e.g. Ennaceur et al., 1997; Mumby et al., 2002) suggest that SOR in which an animal must integrate object identity with spa- lesions to the HPC do not affect exploration of objects in the tial (Aggleton and Nelson, 2020; Bussey et al., 2000; Good et al., sample phase of a SOR task. Also, Gaskin et al. (2010) show that 2007; Save et al., 1992), featural (Good et al., 2007; Mumby sample exploration does not predict test phase performance in et al., 2002) or temporal (Good et al., 2007) information. SOR tasks. Conversely, numerous studies have demonstrated that rodents One of the reasons for conducting our study was the conflict- with hippocampal lesions are not impaired in standard object rec- ing evidence over the role of the HPC in representing environ- ognition (Ainge et al., 2006; Mumby et al., 2002). The results of mental geometry. While experiments with rats seemed to indicate Experiment 1 add to the body of evidence implicating the HPC in that the HPC was necessary for representing local geometric fea- object-location memory, while extending our knowledge of how tures, such as the configuration of long and short walls in a par- location is represented. The results of Experiment 2 confirmed ticular corner (e.g. Jones et al., 2007; McGregor et al., 2004; that the lesions did not affect standard object recognition mem- Pearce et al., 2004), recent research in pigeons (Sotelo et al., ory, while equating some of the procedural and contextual 2019) casts doubt on this conclusion because pigeons showed no changes encountered by rats in Experiment 1. transfer between environments based on local geometry, but hip- As predicted, group Sham discriminated locations with refer- pocampal c-Fos analysis indicated hippocampal activity when ence to the local geometric context in which an object was first pigeons experienced transfer to a familiar overall shape. encountered. The result replicates the findings of Poulter et al. Importantly, the SOR procedure used in our experiments removes (2013), though it should be noted that the current study had a the confound of the nature of the motivational demands of the substantially smaller sample size, so statistical power was procedure since the pigeon study used an appetitive procedure, weaker. One way to ensure that the results in the current study while the rat studies used an aversive motivation. The SOR pro- replicated those of Poulter et al. (2013) is to calculate the replica- cedure also removes the possibility that the previously reported tion Bayes factor (BF), as described by Ly et al. (2019). The effects of HPC lesions on learning based on local geometry were Sham group in Experiment 1 is a direct replication of Poulter because of disruption to the formation of stimulus-response hab- et al.’s (2013) Experiment 2. Therefore, taking a single measure its in the swimming pool, which were reported by Jones et al. of discrimination, the d2 score (novel − familiar/novel + famil- (2007). Our finding that lesions to the HPC disrupted the use of iar), from both Poulter et al.’s (2013) study and the sham data local geometric context for object location in an untrained, nona- from the current study, we calculated the replication BF . This versive procedure provides renewed evidence for the role of the was done by calculating the BF of the combined original and HPC in learning based on local geometry (Pearce et al., 2004). It current d2 scores, compared to a chance level of zero. Following also corresponds with recent evidence from the electrophysiolog- Ly et al. (2019), this combined BF , BF = 17.586, was divided ical literature that changing environmental geometry alters the 10 10 by the BF of the original d2 scores, also compared to chance, local firing patterns of entorhinal grid cells, which are part of the BF = 5.759. The result, BF = 3.05, is the replication BF and hippocampal cognitive mapping system, but that more distant 10 10 10 indicates that the sham data provide evidence for replication grid fields are unaffected by changes to environmental geometry three times greater (precisely, 3.05 times greater) than for the (Krupic et al., 2018). alternative of no replication. We are therefore confident that the However, our results also raise the question of why Sotelo sham results reflect a genuine effect. et al. (2019) were unable to replicate Pearce et al.’s (2004) find- In terms of recognition memory for object location, the results ings, but still found c-Fos activation in the HPC. In terms of the are important in understanding the cues necessary to define a spa- use of local geometry, the use of an appetitive task may have had tial location in recognition memory. In previous object-location an effect. Golob and Taube (2002) reported rats relying more on recognition memory procedures, the location of a familiar object a non-geometric landmark than on environmental geometry is often swapped with that of another or simply displaced (e.g. when motivated by escape from water than when motivated by a Dix and Aggleton, 1999; Good et al., 2007), meaning that both food reinforcer: Cheng’s (1986) original finding that rats prefer- the relative positions of the objects, with reference to other entially relied on geometry over non-geometric features was also objects in the array, and the absolute positions of the objects, with based on an appetitive task (but see Lee et al., 2020 for evidence reference to room cues, could be used to define spatial location that rats in an appetitive reorientation task also coded the non- (see also Langston and Wood, 2010; Wilson et al., 2013, for evi- geometric features of the environment). The differential effect of dence that egocentric strategies may underlie some object-loca- motivation has been also observed in the use of spatial strategies: tion memory). Our results demonstrate that the local geometric Asem and Holland (2013) showed that rats in a water-submerged context in which the object was encountered is sufficient for plus-maze relied on an egocentric response strategy early in object-location recognition memory since both the absolute and training, switching to an allocentric place strategy later, but found relative positions of the objects changed between the exploration the opposite pattern of results when the maze was drained and the and test phases. It should be noted that we did not record explora- escape platform replaced by the opportunity to find food. Turning tion of objects during the sample phase. It might be argued that to Sotelo et al.’s (2019) report of hippocampal c-Fos activation differential group exploration during the sample phase might when pigeons encountered transfer from a rectangle to another Poulter et al. 7 rectangle, but no activation when they transferred from a rectan- an egocentric representation. For example, the position of object gle to a trapezoid, we are only in a position to speculate a reason. A in the kite may have been encoded by remembering that it was One argument is that our lesion study provides stronger evidence to the rat’s left in one right-angled corner, relative to a salient of a causal link between the HPC and object-location memory feature, such as the end of a long wall, while object B was than the correlational nature of IEG activation (Sotelo et al., remembered to the rat’s right in the right-angled corner, relative 2019), though Bingman et al. (2006) showed that hippocampal to the end of the long wall. At test, the unexpected position of lesions impaired pigeons’ reliance on geometric cues. Another object A to the rat’s right at the end of the long wall would have possibility is that there was a discrepancy between the sensitivity caused dishabituation and renewed exploration, but only if the rat of the behavioural task and that of the neural activation, meaning was capable of such an egocentric representation. A number of it was easier to detect changes to IEG expression than it was for possible permutations for this kind of egocentric encoding are behaviour. The possibility also remains that there is a fundamen- possible, but if this is the case then successful object-location tal difference between species in their local and global represen- memory may depend not only on disambiguating long and short tations of space. This possibility seems less likely, however, in walls, involving the HPC, but also coding the object locations light of Tommasi and Polli’s (2004) conclusion that chicks repre- with reference to the positions of long and short walls relative to sent local geometric features rather than global geometry. the rats’ own bodies. To our knowledge, only Korol et al. (2019) Nevertheless, Sotelo et al. (2020) have recently found that the have explored the role of the DLS in a SOR procedure. They terrestrial toad, Rhinella arenarum, also fails to transfer between reported that inactivation of the DLS impaired rats’ memory for a rectangle and kite, and Sotelo et al. (2016) showed that c-Fos the identities of previously encountered objects, but not their activation in the medial pallium of the same species, a putative locations. However, their object-location procedure involved homologue of the mammalian HPC, increased as a result of shifting the positions of two previously encountered objects from exposure to environmental geometry. The possibility of between 40 cm apart to 10 cm apart in an otherwise featureless plexiglass species differences therefore remains. This possibility is made arena. Because objects in our experiment shifted in absolute and greater by the finding that humans are able to use both local and relative positions, only the local geometric context could be used global representations of space (e.g. Buckley et al., 2016, 2019a, to disambiguate objects, which is considerably different from 2019b; Lew et al., 2014; Sturz et al., 2012, 2018), though it Korol et al.’s procedure. should be noted that the role of the HPC in these representations While our results with DLS lesions are novel, their interpreta- has not been investigated. tion does require some speculation which requires further In terms of understanding the nature of the impairments to research. Nevertheless, the results of our experiments provide both the HPC and DLS groups in Experiment 1, it is necessary to further evidence that animals represent the local geometric fea- consider how normal rats represented local geometry. Jones et al. tures of their environment, and that this encoding is automatic, (2007) showed that lesions to the HPC impaired rats’ ability to being evident from recognition memory. This local representa- use the direct metric information provided by wall length. Our tion is impaired by lesions to the HPC, which provides further results for the HPC group are consistent with this finding and support for the argument that HPC-dependent cognitive maps of suggest that sham animals retained their ability to represent the the environment are based on local representations of space. different lengths of walls in the two environments. However, unlike in Jones et al. (2007) our use of an untrained procedure Declaration of conflicting interests prevented sham animals from developing turning habits that The author(s) declared no potential conflicts of interest with respect to seemed to underlie at least some level of successful performance the research, authorship, and/or publication of this article. during training. In Experiment 2, there was no impairment in a standard object recognition task, albeit adapted to control for the Funding context change encountered by rats in Experiment 1. Relevant to the results of Experiment 2, O’Brien et al. (2006) and Piterkin The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was et al. (2008) found that HPC lesions impaired the ability of rats to supported by Biotechnology and Biological Sciences Research Council recognise previously encountered objects when the test context grants to D.J.S. and A.M. 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Journal

Brain and Neuroscience AdvancesSAGE

Published: Nov 17, 2020

Keywords: Spontaneous object recognition; context; geometry; cognitive map; hippocampus; dorsolateral striatum

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