Perirhinal cortex lesions attenuate stimulus generalization in a tactual discrimination task in rats

• Autorzy: Ramos J.M.J.
• Języki publikacji: EN

Abstrakty

EN

Response generalization to a novel stimulus occurs when the new stimulus shares common features with the stimulus used in the original learning. Given the many recent studies suggesting that the perirhinal cortex is critical for disambiguating stimuli that share representational/perceptual elements, we hypothesize that lesions sustained to this region would attenuate response generalization. In the first part of this experiment lesioned and control rats learned a feature-ambiguous tactual discrimination task until they had all reached the same level of performance. In this task animals were asked to discriminate among 3 tactual stimuli simultaneously exposed in 3 arms of a 4-arm plus-shaped maze. In the second part of this experiment, the same rats were given a generalization test 24 h after acquisition of the tactual discrimination. In the generalization test the original tactual stimulus associated with reward during the learning of the discrimination was replaced by a novel tactual stimulus while the other two remained the same. Of the 3 stimuli used in the generalization test, the novel stimulus had the highest degree of feature overlap with respect to the original target stimulus used during the learning of the discrimination. The generalization test took place over two consecutive days, with 8 trials each day. On the first day of generalization, the results indicated that the lesioned rats generalized significantly worse than the control rats during the first 4 trials, but not during the last 4 trials. On the second day of generalization, however, both groups performed the test perfectly. These findings suggest that, in addition to the well-known mnesic function in object processing, the perirhinal cortex may also be involved in perceptual functions.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2014
• Tom: 74
• Numer: 1
• Opis fizyczny: p.15-25,fig.,ref.

Twórcy

autor

Ramos J.M.J.

• Department of Psychobiology and Mind, Brain and Behavior Research Center (CIMCYC), University of Granada, Campus de Cartuja, Granada, Spain

Bibliografia

• Abe H, Ishida Y, Nonaka H, Iwasaki T (2009) Functional difference between rat perirhinal cortex and hippocampus in object and place discrimin ation tasks. Behav Brain Res 197: 388-397.
• Aggleton JP, Albasser MM, Aggleton DJ, Poirier GL, Pearce JM (2010) Lesions of the rat perirhinal cortex spare the acquisition of a complex configural visual discrimination yet impair object recognition. Behav Neurosci 124: 55-68.
• Agster KL, Burwell RD (2009) Cortical efferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. Hippocampus 19: 1159-1186.
• Barense MD, Groen IIA, Lee ACH, Yeung L-K, Brady SM, Gregori M, Kapur N, Bussey TJ, Saksida LM, Henson RNA (2012) Intact memory for irrelevant information impairs perception in amnesia. Neuron 75: 157-167.
• Bartko SJ, Winters BD, Cowell RA, Saksida LM, Bussey TJ (2007) Perceptual functions of perirhinal cortex in rats: zero-delay object recognition and simultaneous oddity discriminations. J Neurosci 27: 2548-2559.
• Baxter M (2009) Involvement of medial temporal lobe struc¬tures in memory and perception. Neuron 61: 667-677.
• Brown MW, Warburton EC, Aggleton JP (2010) Recognition memory: Material, processes, and substrates. Hippocampus 20: 1228-1244.
• Buckley MJ, Gaffan D (1998) Perirhinal cortex ablation impairs visual object identification. J Neurosci 18: 2268¬2275.
• Buckley MJ, Gaffan D (2006) Perirhinal cortical contribu¬tions to object perception. Trends Cogn Sci 10: 100¬107.
• Buckley MJ, Gaffan D, Murray EA (1997) Functional dou¬ble dissociation between two inferior temporal cortical areas: Perirhinal cortex versus middle temporal gyrus. J Neurophysiol 77: 587-598.
• Buckley MJ, Booth MC, Rolls ET, Gaffan D (2001) Selective perceptual impairments after perirhinal cortex ablation. J Neurosci 21: 9824-9836.
• Burwell RD (2001) Borders and cytoarchitecture of the per- irhinal and postrhinal cortices in the rat. J Comp Neurol 437: 17-41.
• Burwell RD, Amaral DC (1998) Cortical afferents of the perirhinal, postrhinal and entorhinal cortices of the rat. J Comp Neurol 398: 179-205.
• Burwell RD, Witter MP, Amaral DC (1995) Perirhinal and postrhinal cortices of the rat: A review of the neuroanatomical literature and comparison with findings from the monkey brain. Hippocampus 5: 390-408.
• Bussey TJ, Saksida LM (2002) The organization of visual object representations: a connectionist model of effects of lesions in perirhinal cortex. Eur J Neurosci 15: 353-364.
• Bussey TJ, Saksida LM (2005) Object memory and percep¬tion in the medial temporal lobe: An alternative approach. Curr Opin Neurobiol 15: 730-737.
• Bussey TJ, Saksida LM, Murray EA (2002) Perirhinal cortex resolves feature ambiguity in complex visual discrimina¬tions. Eur J Neurosci 15: 365-374.
• Bussey TJ, Saksida LM, Murray EA (2003) Impairments in visual discrimination after perirhinal cortex lesions: Testing 'declarative' vs. 'perceptual-mnemonic' views of perirhinal cortex function. Eur J Neurosci 17: 649-660.
• Campolattaro MM, Freeman JH (2006) Perirhinal cortex lesions impair feature-negative discrimination. Neurobiol Learn Mem 86: 205-213.
• Clark RE, Reinagel P, Broadbent NJ, Flister ED, Squire LR (2011) Intact performance on feature-ambiguous dis¬criminations in rats with lesions of the perirhinal cortex. Neuron 70: 132-140.
• Cowell RA, Bussey TJ, Saksida LM (2006) Why does brain damage impair memory? A connectionist model of object recognition memory in perirhinal cortex. J Neurosci 26: 12186-12197.
• Eacott MJ, Gaffan EA (2005) The roles of perirhinal cortex, postrhinal cortex, and the fornix in memory for objects, con¬texts, and events in the rat. Q J Exp Psychol 58B: 202-217.
• Eacott MJ, Gaffan D, Murray EA (1994) Preserved recogni¬tion memory for small sets, and impaired stimulus identi¬fication for large sets, following rhinal cortex ablations in monkeys. Eur J Neurosci 6: 1466-1478.
• Eacott MJ, Machin PE, Gaffan EA (2001) Elemental and configural visual discrimination learning following lesions to perirhinal cortex in the rat. Behav Brain Res 124: 55-70.
• Eichenbaum H, Yonelinas AP, Ranganath C (2007) The medial temporal lobe and recognition memory. Annu Rev Neurosci 30: 123-152.
• Feinberg LM, Allen TA, Ly D, Fortin NJ (2012) Recognition memory for social and non-social odors: Differential effects of neurotoxic lesions to the hippocampus and per- irhinal cortex. Neurobiol Learn Mem 97: 7-16.
• Gilbert PE, Kesner RP (2003) Recognition memory for com¬plex visual discriminations is influenced by stimulus interference in rodents with perirhinal cortex damage. Learn Mem 10: 525-530.
• Goulet S, Murray EA (2001) Neural substrates of crossmodal association memory in monkeys: The amygdala versus the anterior rhinal cortex. Behav Neurosci 115: 271-284.
• Hampton RR, Murray EA (2002) Learning of discrimina¬tions is impaired, but generalization to altered views is intact, in monkeys (Macaca mulatta) with perirhinal cor¬tex removal. Behav Neurosci 116: 363-377.
• Harris JA (2006) Elemental representations of stimuli in associative learning. Psychol Rev 113: 584-605.
• Holdstock JS, Hocking J, Notley P, Devlin JT, Price CJ (2009) Integrating visual and tactile information in the perirhinal cortex. Cereb Cortex 29: 2993-3000.
• Hunsaker MR, Kesner RP (2013) The operation of pattern separation and pattern completion processes associated with different attributes or domains of memory. Neurosci Biobehav Rev 37: 36-58.
• Johnson KO (2001) The roles and functions of cutaneous mechanoreceptors. Curr Opin Neurobiol 11: 455-461.
• Kealy J, Commins S (2011) The rat perirhinal cortex: A review of anatomy, physiology, plasticity and function. Prog Neurobiol 93: 522-548.
• Kholodar-Smith DB, Allen TA, Brown TH (2008) Fear con¬ditioning to discontinuous auditory cues requires perirhinal cortical function. Behav Neurosci 122: 1178-1185.
• Kim S, Jeneson A, van der Horst A, Frascino J, Hopkins RO, Squire LR (2011) Memory, visual discrimination perfor¬mance and the human hippocampus. J Neurosci 31: 2624-2629.
• Kivisaari SL, Tyler LK, Monsch AU, Taylor KI (2012) Medial perirhinal cortex disambiguates confusable objects. Brain 135: 3757-3769.
• Lindquist DH, Jarrard LE, Brown TH (2004) Perirhinal cor¬tex supports delay fear conditioning to rat ultrasonic social signals. J Neurosci 24: 3610-3617.
• Mackintosh NJ (1974) The Psychology of Animal Learning. Academic Press, London, UK.
• Malkova L, Mishkin M (2003) One-trial memory for object- place associations after separate lesions of hippocampus and posterior parahippocampal region in the monkey J Neurosci 23: 1956-1965.
• Maricich SM, Morrison KM, Mathes EL, Brewer BM (2012) Rodents rely on merkel cells for texture discrimi¬nation tasks. J Neurosci 32: 3296-3300.
• Mullally SL, Maguire EA (2011) A new role for parahip- pocampal cortex in representing space. J Neurosci 31: 7441-7449.
• Murray EA, Bussey TJ, Hampton RR, Saksida LM (2000) The parahippocampal region and object identification. Ann N Y Acad Sci 911: 166-174.
• Murray EA, Bussey TJ, Saksida LM (2007) Visual percep¬tion and memory: A new view of medial temporal lobe function in primates and rodents. Annu Rev Neurosci 30: 99-122.
• Norman G, Eacott MJ (2004) Impaired object recogni¬tion with increasing levels of feature ambiguity in rats with perirhinal cortex lesions. Behav Brain Res 148: 79-91.
• Norman G, Eacott MJ (2005) Dissociable effects of lesions to the perirhinal cortex and the postrhinal cortex on memory for context and objects in rats. Behav Neurosci 119: 557-566.
• Paxinos G, Watson C (1998) The Rat Brain in Stereotaxic Coordinates (4th ed.). Academic Press, New York, NY.
• Ramos JMJ (2013a) Essential role of the perirhinal cortex in complex tactual discrimination tasks in rats. Cereb Cortex (E-pub ahead of Print). [doi: 10.1093/cercor/bht054.]
• Ramos JMJ (2013b) Differential contribution of hippocam¬pus, perirhinal cortex and postrhinal cortex to allocentric spatial memory in the radial maze. Behav Brain Res 247: 59-64.
• Robinson J, Whitt EJ, Horsley RR, Jones PM (2010) Familiarity-based stimulus generalization of conditioned supression in rats is dependent on the perirhinal cortex. Behav Neurosci 124: 587-599.
• Saksida LM, Bussey TJ (2010) The representational-hierar¬chical view of amnesia: Translation from animal to human. Neuropsychologia 48: 2370-2384.
• Shrager Y, Gold JJ, Hopkins RO, Squire LR (2006) Intact visual perception in memory-impaired patients with medial temporal lobe lesions. J Neurosci 26: 2235-2240.
• Squire LR, Zola-Morgan S (1991) The medial temporal lobe memory system. Science 253: 1380-1386.
• Suzuki WA (2009) Perception and the medial temporal lobe: Evaluating the current evidence. Neuron 61: 657-666.
• Suzuki WA (2010) Untangling memory from perception in the medial temporal lobe. Trends Cogn Sci 14: 195-200.
• Suzuki WA, Amaral DG (1994) Perirhinal and parahip- pocampal cortices of the macaque monkey: Cortical afferents. J Comp Neurol 350: 497-533.
• Suzuki WA, Baxter MG (2009) Memory, perception, and the medial temporal lobe: A synthesis of opinions. Neuron 61: 678-679.
• Taylor KI, Moss HE, Stamatakis EA, Tyler LK (2006) Binding crossmodal object features in perirhinal cortex. Proc Natl Acad Sci U S A 103: 8239-8244.
• Wagner AR (2003) Context-sensitive elemental theory. Q J Exp Psychol B 56: 7-29.
• Watson HC, Lee ACH (2013) The perirhinal cortex and recognition memory interference. J Neurosci 33: 4192-4200.
• Winters BD, Reid JM (2010) A distributed cortical represen¬tation underlies crossmodal object recognition in rats. J Neurosci 30: 6253-6261.
• Wu HPP, Ioffe JC, Iverson MM, Boon JM, Dyck RH (2013) Novel, whisker-dependent texture discrimination task for mice. Behav Brain Res 237: 238-242.
• Yonelinas AP, Aly M, Wang WC, Koen JD (2010) Recollection and familiarity: examining controversial assumptions and new directions. Hippocampus 20: 1178-1194.