{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,2]],"date-time":"2026-09-02T22:55:14Z","timestamp":1788389714776,"version":"build-2803163510"},"reference-count":37,"publisher":"IMR Press","issue":"11","license":[{"start":{"date-parts":[[2024,11,18]],"date-time":"2024-11-18T00:00:00Z","timestamp":1731888000000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Natural Sciences and Engineering Research Council of Canada grant","award":["RGPIN-2020-06929"],"award-info":[{"award-number":["RGPIN-2020-06929"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["J. Integr. Neurosci."],"abstract":"<jats:p>Background: The goal of these experiments was to determine which learning and memory system(s) were necessary for the retention of visual discriminations and subsequent acquisition of a second problem. The dorsal striatum should be involved in the acquisition and expression of this task based on previous work implicating this region in instrumental learning and memory processes. The perirhinal cortex has been implicated in learning and memory processes associated with visual information like objects, and pictures and may also play a role in the acquisition and\/or retention of visual discriminations. As there is no clear spatial\/relational component to the task, the hippocampus should not be involved. Methods: Rats were trained on a two-choice visual discrimination task to criterion performance after which they received lesions to portions of the dorsal striatum (dorso-medial or dorso-lateral striatum) and medial temporal lobe (perirhinal cortex or hippocampus). After surgical recovery, the rats were tested for retention of the original discrimination, followed by training on a second problem on the same task. Results: The results showed that dorsal medial striatal lesions produced a retrograde deficit on picture discrimination, but dorsal lateral striatum lesions did not. Neither dorsal striatal lesion produced a deficit on acquisition of a second problem. Perirhinal cortex did not seem to make an essential contribution to the retention of the original discrimination or acquisition of the second problem. Surprisingly, subjects with hippocampal damage were severely impaired but eventually re-learned the discrimination. Damage to the hippocampus had no impact on acquisition of a second problem. Conclusions: Taken together, the results of the present experiments show that the dorsomedial striatum and the hippocampus may support performance on this instrumental task if intact during acquisition but is not required for acquisition of a new problem. The implications of this pattern of results for our understanding of the organization of learning and memory in mammals is discussed.<\/jats:p>","DOI":"10.31083\/j.jin2311205","type":"journal-article","created":{"date-parts":[[2024,11,27]],"date-time":"2024-11-27T11:34:00Z","timestamp":1732707240000},"source":"Crossref","is-referenced-by-count":3,"title":["Anterograde versus Retrograde Effects of Damage to Identified Learning and Memory Systems during Acquisition, Retention, and Re-Acquisition of an Instrumental Visual Discrimination Task: Dorsal Striatum, Perirhinal Cortex, and Hippocampus"],"prefix":"10.31083","volume":"23","author":[{"given":"Robert J.","family":"McDonald","sequence":"first","affiliation":[{"name":"Canadian Centre for Behavioural Neuroscience, Department of Neuroscience, University of Lethbridge, Lethbridge, AB T1K 3M4, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joelle","family":"Kopp","sequence":"first","affiliation":[{"name":"Canadian Centre for Behavioural Neuroscience, Department of Neuroscience, University of Lethbridge, Lethbridge, AB T1K 3M4, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Erin L.","family":"Zelinski","sequence":"first","affiliation":[{"name":"Canadian Centre for Behavioural Neuroscience, Department of Neuroscience, University of Lethbridge, Lethbridge, AB T1K 3M4, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert J.","family":"Sutherland","sequence":"first","affiliation":[{"name":"Canadian Centre for Behavioural Neuroscience, Department of Neuroscience, University of Lethbridge, Lethbridge, AB T1K 3M4, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hugo","family":"Lehmann","sequence":"first","affiliation":[{"name":"Department of Psychology, Trent University, Peterborough, ON K9L 0G2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fraser","family":"Sparks","sequence":"first","affiliation":[{"name":"Regeron Pharmaceuticals, Bronx, NY 10591, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nancy S.","family":"Hong","sequence":"first","affiliation":[{"name":"Canadian Centre for Behavioural Neuroscience, Department of Neuroscience, University of Lethbridge, Lethbridge, AB T1K 3M4, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"16242","published-online":{"date-parts":[[2024,11,18]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","unstructured":"White NM, McDonald RJ. Multiple parallel memory systems in the brain of the rat. Neurobiology of Learning and Memory. 2002; 77: 125\u2013184.","DOI":"10.1006\/nlme.2001.4008"},{"key":"ref2","doi-asserted-by":"crossref","unstructured":"Bagshaw MH, Benzies S. Multiple measures of the orienting reaction and their dissociation after amygdalectomy in monkeys. Experimental Neurology. 1968; 20: 175\u2013187.","DOI":"10.1016\/0014-4886(68)90090-3"},{"key":"ref3","doi-asserted-by":"crossref","unstructured":"Everitt BJ, Morris KA, O\u2019Brien A, Robbins TW. The basolateral amygdala-ventral striatal system and conditioned place preference: further evidence of limbic-striatal interactions underlying reward-related processes. Neuroscience. 1991; 42: 1\u201318.","DOI":"10.1016\/0306-4522(91)90145-E"},{"key":"ref4","doi-asserted-by":"crossref","unstructured":"Hiroi N, White NM. The lateral nucleus of the amygdala mediates expression of the amphetamine-produced conditioned place preference. The Journal of Neuroscience. 1991; 11: 2107\u20132116.","DOI":"10.1523\/JNEUROSCI.11-07-02107.1991"},{"key":"ref5","doi-asserted-by":"crossref","unstructured":"Kapp BS, Frysinger RC, Gallagher M, Haselton JR. Amygdala central nucleus lesions: effect on heart rate conditioning in the rabbit. Physiology & Behavior. 1979; 23: 1109\u20131117.","DOI":"10.1016\/0031-9384(79)90304-4"},{"key":"ref6","doi-asserted-by":"crossref","unstructured":"Packard MG, Hirsh R, White NM. Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems. The Journal of Neuroscience. 1989; 9: 1465\u20131472.","DOI":"10.1523\/JNEUROSCI.09-05-01465.1989"},{"key":"ref7","doi-asserted-by":"crossref","unstructured":"Corcoran KA, Maren S. Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction. The Journal of Neuroscience. 2001; 21: 1720\u20131726.","DOI":"10.1523\/JNEUROSCI.21-05-01720.2001"},{"key":"ref8","doi-asserted-by":"crossref","unstructured":"Morris RG, Garrud P, Rawlins JN, O\u2019Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature. 1982; 297: 681\u2013683.","DOI":"10.1038\/297681a0"},{"key":"ref9","doi-asserted-by":"crossref","unstructured":"Rudy JW, Barrientos RM, O\u2019Reilly RC. Hippocampal formation supports conditioning to memory of a context. Behavioral Neuroscience. 2002; 116: 530\u2013538.","DOI":"10.1037\/\/0735-7044.116.4.530"},{"key":"ref10","doi-asserted-by":"crossref","unstructured":"Brown MW, Aggleton JP. Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nature Reviews. Neuroscience. 2001; 2: 51\u201361.","DOI":"10.1038\/35049064"},{"key":"ref11","doi-asserted-by":"crossref","unstructured":"Mumby DG, Pinel JP. Rhinal cortex lesions and object recognition in rats. Behavioral Neuroscience. 1994; 108: 11\u201318.","DOI":"10.1037\/\/0735-7044.108.1.11"},{"key":"ref12","doi-asserted-by":"crossref","unstructured":"Dickinson A. Instrumental conditioning. In Mackintosh NJ, (ed.) Animal Cognition and Learning. Academy Press: London. 1994.","DOI":"10.1016\/B978-0-08-057169-0.50009-7"},{"key":"ref13","doi-asserted-by":"crossref","unstructured":"Devan BD, Hong NS, McDonald RJ. Parallel associative processing in the dorsal striatum: segregation of stimulus-response and cognitive control subregions. Neurobiology of Learning and Memory. 2011; 96: 95\u2013120.","DOI":"10.1016\/j.nlm.2011.06.002"},{"key":"ref14","doi-asserted-by":"crossref","unstructured":"Balleine BW, Liljeholm M, Ostlund SB. The integrative function of the basal ganglia in instrumental conditioning. Behavioural Brain Research. 2009; 199: 43\u201352.","DOI":"10.1016\/j.bbr.2008.10.034"},{"key":"ref15","doi-asserted-by":"crossref","unstructured":"O\u2019Keefe J, Nadel L, Keightley S, Kill D. Fornix lesions selectively abolish place learning in the rat. Experimental Neurology. 1975; 48: 152\u2013166.","DOI":"10.1016\/0014-4886(75)90230-7"},{"key":"ref16","doi-asserted-by":"crossref","unstructured":"Epp J, Keith JR, Spanswick SC, Stone JC, Prusky GT, Sutherland RJ. Retrograde amnesia for visual memories after hippocampal damage in rats. Learning & Memory (Cold Spring Harbor, N.Y.). 2008; 15: 214\u2013221.","DOI":"10.1101\/lm.788008"},{"key":"ref17","doi-asserted-by":"crossref","unstructured":"Yin HH, Ostlund SB, Knowlton BJ, Balleine BW. The role of the dorsomedial striatum in instrumental conditioning. The European Journal of Neuroscience. 2005; 22: 513\u2013523.","DOI":"10.1111\/j.1460-9568.2005.04218.x"},{"key":"ref18","doi-asserted-by":"crossref","unstructured":"Yin HH, Knowlton BJ, Balleine BW. Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. The European Journal of Neuroscience. 2004; 19: 181\u2013189.","DOI":"10.1111\/j.1460-9568.2004.03095.x"},{"key":"ref19","doi-asserted-by":"crossref","unstructured":"Featherstone RE, McDonald RJ. Lesions of the dorsolateral striatum impair the acquisition of a simplified stimulus-response dependent conditional discrimination task. Neuroscience. 2005; 136: 387\u2013395.","DOI":"10.1016\/j.neuroscience.2005.08.021"},{"key":"ref20","doi-asserted-by":"crossref","unstructured":"Gruber AJ, McDonald RJ. Context, emotion, and the strategic pursuit of goals: interactions among multiple brain systems controlling motivated behavior. Frontiers in Behavioral Neuroscience. 2012; 6: 50.","DOI":"10.3389\/fnbeh.2012.00050"},{"key":"ref21","doi-asserted-by":"crossref","unstructured":"McDonald RJ, Devan BD, Hong NS. Multiple memory systems: the power of interactions. Neurobiology of Learning and Memory. 2004; 82: 333\u2013346.","DOI":"10.1016\/j.nlm.2004.05.009"},{"key":"ref22","unstructured":"Tolman EC. Purposive Behavior in animals and man. Appleton: New York. 1932."},{"key":"ref23","doi-asserted-by":"crossref","unstructured":"Meyer-Mueller C, Jacob PY, Montenay JY, Poitreau J, Poucet B, Chaillan FA. Dorsal, but not ventral, hippocampal inactivation alters deliberation in rats. Behavioural Brain Research. 2020; 390: 112622.","DOI":"10.1016\/j.bbr.2020.112622"},{"key":"ref24","doi-asserted-by":"crossref","unstructured":"Kealy J, Commins S. The rat perirhinal cortex: A review of anatomy, physiology, plasticity, and function. Progress in Neurobiology. 2011; 93: 522\u2013548.","DOI":"10.1016\/j.pneurobio.2011.03.002"},{"key":"ref25","doi-asserted-by":"crossref","unstructured":"Winters BD, Bussey TJ. Transient inactivation of perirhinal cortex disrupts encoding, retrieval, and consolidation of object recognition memory. The Journal of Neuroscience. 2005; 25: 52\u201361.","DOI":"10.1523\/JNEUROSCI.3827-04.2005"},{"key":"ref26","doi-asserted-by":"crossref","unstructured":"Zola-Morgan S, Squire LR, Amaral DG, Suzuki WA. Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. The Journal of Neuroscience. 1989; 9: 4355\u20134370.","DOI":"10.1523\/JNEUROSCI.09-12-04355.1989"},{"key":"ref27","doi-asserted-by":"crossref","unstructured":"Aggleton JP, Keen S, Warburton EC, Bussey TJ. Extensive cytotoxic lesions involving both the rhinal cortices and area TE impair recognition but spare spatial alternation in the rat. Brain Research Bulletin. 1997; 43: 279\u2013287.","DOI":"10.1016\/S0361-9230(97)00007-5"},{"key":"ref28","doi-asserted-by":"crossref","unstructured":"Winters BD, Bartko SJ, Saksida LM, Bussey TJ. Muscimol, AP5, or scopolamine infused into perirhinal cortex impairs two-choice visual discrimination learning in rats. Neurobiology of Learning and Memory. 2010; 93: 221\u2013228.","DOI":"10.1016\/j.nlm.2009.10.002"},{"key":"ref29","doi-asserted-by":"crossref","unstructured":"Lee JQ, Zelinski EL, McDonald RJ, Sutherland RJ. Heterarchic reinstatement of long-term memory: A concept on hippocampal amnesia in rodent memory research. Neuroscience and Biobehavioral Reviews. 2016; 71: 154\u2013166.","DOI":"10.1016\/j.neubiorev.2016.08.034"},{"key":"ref30","doi-asserted-by":"crossref","unstructured":"Clarke HA, Skinner DM, van der Kooy D. Combined hippocampal and amygdala lesions block learning of a response-independent form of occasion setting. Behavioral Neuroscience. 2001; 115: 341\u2013357.","DOI":"10.1037\/\/0735-7044.115.2.341"},{"key":"ref31","doi-asserted-by":"crossref","unstructured":"McDonald RJ, Jones J, Richards B, Hong NS. A double dissociation of dorsal and ventral hippocampal function on a learning and memory task mediated by the dorso-lateral striatum. The European Journal of Neuroscience. 2006; 24: 1789\u20131801.","DOI":"10.1111\/j.1460-9568.2006.05064.x"},{"key":"ref32","doi-asserted-by":"crossref","unstructured":"Lehmann H, Stykel MG, Glenn MJ. Overtraining Strengthens the Visual Discrimination Memory Trace Outside the Hippocampus in Male Rats. Frontiers in Behavioral Neuroscience. 2021; 15: 768552.","DOI":"10.3389\/fnbeh.2021.768552"},{"key":"ref33","doi-asserted-by":"crossref","unstructured":"Devan BD, White NM. Parallel information processing in the dorsal striatum: relation to hippocampal function. The Journal of Neuroscience. 1999; 19: 2789\u20132798.","DOI":"10.1523\/JNEUROSCI.19-07-02789.1999"},{"key":"ref34","doi-asserted-by":"crossref","unstructured":"Sutherland RJ, Lee JQ, McDonald RJ, Lehmann H. Has multiple trace theory been refuted? Hippocampus. 2020; 30: 842\u2013850.","DOI":"10.1002\/hipo.23162"},{"key":"ref35","doi-asserted-by":"crossref","unstructured":"McDonald RJ, Ko CH, Hong NS. Attenuation of context-specific inhibition on reversal learning of a stimulus-response task in rats with neurotoxic hippocampal damage. Behavioural Brain Research. 2002; 136: 113\u2013126.","DOI":"10.1016\/S0166-4328(02)00104-3"},{"key":"ref36","doi-asserted-by":"crossref","unstructured":"McDonald RJ, Balog RJ, Lee JQ, Stuart EE, Carrels BB, Hong NS. Rats with ventral hippocampal damage are impaired at various forms of learning including conditioned inhibition, spatial navigation, and discriminative fear conditioning to similar contexts. Behavioural Brain Research. 2018; 351: 138\u2013151.","DOI":"10.1016\/j.bbr.2018.06.003"},{"key":"ref37","doi-asserted-by":"crossref","unstructured":"McDonald RJ, Yim TT, Lehmann H, Sparks FT, Zelinski EL, Sutherland RJ, et al. Expression of a conditioned place preference or spatial navigation task following muscimol-induced inactivations of the amygdala or dorsal hippocampus: A double dissociation in the retrograde direction. 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