Skip to main content
Log in

The role of medial prefrontal cortex in context-specific inhibition during reversal learning of a visual discrimination

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Rats with medial prefrontal cortex or sham lesions were trained on a visual discrimination task designed for the eight-arm radial maze. After reaching asymptotic performance on this task, both groups were divided into sub-groups that would experience reversal learning in the same or different context from original training. The results showed that both groups reversed in the different context had accelerated learning compared to the groups reversed in the same context. Reversal learning in rats with medial prefrontal cortex damage was faster than sham animals in the same context. These and other results from a transfer test suggest that the medial prefrontal cortex participates in the behavioral effects of a context-specific inhibitory association acquired during visual discrimination learning.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Ashe J, Lungu OV, Basford AT, Lu X (2006) Cortical control of motor sequences. Curr Opin Neurobiol 16:213–221

    Article  PubMed  CAS  Google Scholar 

  • Birell JM, Brown VJ (2000) Medial frontal cortex mediates perceptual attentional set shifting in the rat. J Neurosci 20:4320–4324

    Google Scholar 

  • Blum S, Hebert AE, Dash PK (2006) A role for the prefrontal cortex in recall of recent and remote memories. Neuroreport 17:341–344

    Article  PubMed  Google Scholar 

  • Bouton M, Brooks DC (1993) Time and context effects on performance in a pavlovian discrimination reversal. J Exp Psychol Anim Behav Process 19:165–179

    Article  Google Scholar 

  • Castelo JM, Sherman SJ, Courtney MG, Melrose RJ, Stern CE (2006) Altered hippocampal-prefrontal activation in HIV patients during episodic memory encoding. Neurology 66:1688–1695

    Article  PubMed  CAS  Google Scholar 

  • Chudasama Y, Robbins TW (2003) Dissociable contributions of the orbitofrontal and infralimbic cortex to pavlovian autoshaping and discrimination reversal learning: further evidence for the functional heterogeneity of the rodent frontal cortex. J Neurosci 23:8771–8780

    PubMed  CAS  Google Scholar 

  • De Bruin JPC, Swinkels WAM, de Brabander JM (1997) Response learning of rats in a Morris water maze: involvement of the medial prefrontal cortex. Behav Brain Res 85:47–55

    Article  PubMed  Google Scholar 

  • Delatour B, Gisquet-Verrier P (1999) Lesions of the prelimbic-infralimbic cortices in rats do not disrupt response selection processes but induce delay-dependent deficits: evidence for a role in working memory? Behav Neurosci 113:941–955

    Article  PubMed  CAS  Google Scholar 

  • Dias R, Robbins TW, Roberts AC (1996) Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380:69–72

    Article  PubMed  CAS  Google Scholar 

  • Divac I (1968) Functions of the caudate nucleus. Acta Biol Exp (Warsaw) 28:107–120

    CAS  Google Scholar 

  • Gemmell C, O’Mara SM (1999) Medial prefrontal cortex lesions cause deficits in a variable-goal location task but not in object exploration. Behav Neurosci 113:465–474

    Article  PubMed  CAS  Google Scholar 

  • Granon S, Poucet B (2000) Involvement of the rat prefrontal cortex in cognitive functions: a central role for the prelimbic area. Psychobiology 28:229–237

    Google Scholar 

  • Honey RC, Good M (1993) Selective hippocampal lesions abolish the contextual specificity of latent inhibition and conditioning. Behav Neurosci 107:23–33

    Article  PubMed  CAS  Google Scholar 

  • Holt W, Maren S (1999) Muscimol inactivation of the dorsal hippocampus impairs contextual retrieval of fear memory. J Neurosci 19:9054–9062

    PubMed  CAS  Google Scholar 

  • Joel D, Weiner I, Feldon J (1997) Electrolytic lesions of the medial prefrontal cortex in rats disrupt performance on an analog of the Wisconsin Card Sorting Test, but do not disrupt latent inhibition: implications for animal models of schizophrenia. Behav Brain Res 85:187–201

    Article  PubMed  CAS  Google Scholar 

  • Kapp BS, Gallagher M, Holmquist BK, Theall CL (1979) Amygdala central nucleus lesions: effect on heart rate conditioning in the rabbit. Physiol Behav 23:1109–1117

    Article  PubMed  CAS  Google Scholar 

  • Killcross S, Coutureau E (2003) Coordination of actions and habits in the medial prefrontal cortex in rats. Cereb Cortex 13:400–408

    Article  PubMed  Google Scholar 

  • King JA, Hartley T, Spiers HJ, Maguire EA, Burgess N (2005) Anterior prefrontal involvement in episodic retrieval reflects contextual interference. Neuroimage 28:256–267

    Article  PubMed  CAS  Google Scholar 

  • Kolb B (1984) Functions of the prefrontal cortex in the rat: a comparative review. Brain Res Rev 8:65–98

    Article  Google Scholar 

  • Kolb B, Burhman K, McDonald RJ, Sutherland RJ (1994) Dissociation of the medial prefrontal, posterior parietal and posterior temporal cortex for spatial navigation and recognition memory in the rat. Cereb Cortex 6:664–680

    Article  Google Scholar 

  • Lacroix L, Broersen LM, Weiner I, Feldon J (1998) The effects of excitotoxic lesion of the medial prefrontal cortex on latent inhibition, prepulse inhibition, food hoarding, elevated plus maze, active avoidance and locomotor activity in the rat. Neuroscience 82:431–442

    Article  Google Scholar 

  • Liston C, Miller MM, Goldwater DS, Radley JJ, Roceher AB, Hof PR, Morrison JH, McEwen BS (2006) Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci 26:7870–7874

    Article  PubMed  CAS  Google Scholar 

  • Marshuetz C, Smith EE (2006) Working memory for order information: multiple cognitive and neural mechanisms. Neuroscience 139:195–200

    Article  PubMed  CAS  Google Scholar 

  • McDonald RJ, Hong NS, Devan BD (2004) The challenges of understanding mammalian cognition and memory-based behaviours: an interacting learning and memory systems approach. Neurosci Biobehav Rev 28 (7):719–746

    Article  PubMed  Google Scholar 

  • McDonald RJ, King AL, Hong NS (2001) Context-specific interference on reversal learning of a stimulus-response habit. Behav Brain Res 121:149–165

    Article  PubMed  CAS  Google Scholar 

  • McDonald RJ, Ko C, Hong NS (2002) Attenuation of context-specific inhibition on reversal learning of a stimulus-response task in rats with neurotoxic hippocampal damage. Behav Brain Res 136:113–126

    Article  PubMed  Google Scholar 

  • McDonald RJ, White NM (1993) A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum. Behav Neurosci 107:3–22

    Article  PubMed  CAS  Google Scholar 

  • Mimura M, Yano M (2006) Memory impairment and awareness of memory deficits in early-stage Alzheimer’s disease. Rev Neurosci 17:253–266

    PubMed  Google Scholar 

  • Moscovitch M (1992) Memory and working-with-memory: a component process model based on modules and central systems. J Cognit Neurosci 4:258–267

    Article  Google Scholar 

  • Mumby DG, Pinel JPJ (1994) Rhinal cortex lesions and object recognition in rats. Behav Neurosci 108:11–18

    Article  PubMed  CAS  Google Scholar 

  • Narayanan NS, Horst NK, Laubach M (2006) Reversible inactivations of rat medial prefrontal cortex impair the ability to wait for a stimulus. Neuroscience 139:865–876

    Article  PubMed  CAS  Google Scholar 

  • O’Keefe JA, Nadel L, Keightley S, Kill D (1975) Fornix lesions selectively abolish place learning in the rat. Exp Neurol 48:152–166

    Article  PubMed  CAS  Google Scholar 

  • Packard MG, Hirsh R, White NM (1989) Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems. J Neurosci 9:1465–1472

    PubMed  CAS  Google Scholar 

  • Paxinos G, Watson C (1998) The rat brain atlas in stereotaxic coordinates, 4th edn. Academic Press, San Diego, CA

    Google Scholar 

  • Powell DA, Ginsberg JP (2005) Single unit activity in the medial prefrontal cortex during Pavlovian heart rate conditioning: effects of peripheral autonomic blockade. Neurobiol Learn Mem 84:200–213

    Article  PubMed  CAS  Google Scholar 

  • Quirk GJ, Garcia R, Gonzalez-Lima F (2006) Prefrontal mechanisms in extinction of conditioned fear. Biol Psychiatry 60:337–343

    Article  PubMed  Google Scholar 

  • Ragozzino ME, Detrick S, Kesner RP (1999a) Involvement of the pre-limbic-infralimbic areas of the rodent prefrontal cortex in behavioral flexibility for place and response learning. J Neurosci 19:4585–4594

    CAS  Google Scholar 

  • Ragozzino ME, Wilcox C, Raso M, Kesner RP (1999b) Involvement of rodent prefrontal cortex subregions in strategy switching. Behav Neurosci 113:32–41

    Article  CAS  Google Scholar 

  • Ranganath C (2006) Working memory for visual objects: complementary roles of inferior temporal, medial temporal, and prefrontal cortex. Neuroscience 139:277–289

    Article  PubMed  CAS  Google Scholar 

  • Reep R (1984) Relationship between prefrontal and limbic cortex: a comparative anatomical review. Brain Behav Evol 25:1–80

    Google Scholar 

  • Sage JR, Knowlton BJ (2000) Effects of US devaluation on win-stay and win-shift radial maze performance in rats. Behav Neurosci 114:295–306

    Article  PubMed  CAS  Google Scholar 

  • Schwartzbaum JS, Poulos DA (1965) Discrimination behavior after amygdalectomy in monkeys: learning set and discrimination reversals. J Comp Physiol Psychol 320–328

  • Simons JS, Owen AM, Fletcher PC, Burgess PW (2005) Anterior prefrontal cortex and the recollection of contextual information. Neuropsychologia 43:1774–1783

    Article  PubMed  Google Scholar 

  • Sutherland RJ, Kolb B, Whishaw IQ (1982) Definitive disruption by hippocampal and medial frontal cortical damage in the rat. Neurosci Lett 31:271–276

    Article  PubMed  CAS  Google Scholar 

  • Thompson RF (1990) Neural mechanisms of classical conditioning in mammals. Philosophical Transactions of the Royal Society of London. B: Biol Sci 329:161–170

    CAS  Google Scholar 

  • Thomas DR, McKelvie AR, Ranney M, Moye TB (1981) Interference in pigeons’ long-term memory viewed as a retrieval problem. Anim Learn Behav 9:581–586

    Google Scholar 

  • White NM, McDonald RJ (2002) Multiple parallel memory systems in the brain of the rat. Neurobiol Learn Mem 77:125–184

    Article  PubMed  Google Scholar 

  • Wise SP, Murray EA, Gerfen CR (1996) The frontal cortex-basal ganglia system in primates. Crit Rev Neurobiol 10:317–356

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Dr. Robert McDonald is currently a Canada Research Chair. This research was supported by grants awarded to RJM from the Canadian Stroke Network and the Natural Sciences and Engineering Research Council. We would like to thank Dr. Bryan Kolb for sharing his expertise on the anatomy of the rat prefrontal cortex.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. J. McDonald.

Rights and permissions

Reprints and permissions

About this article

Cite this article

McDonald, R.J., Foong, N., Ray, C. et al. The role of medial prefrontal cortex in context-specific inhibition during reversal learning of a visual discrimination. Exp Brain Res 177, 509–519 (2007). https://doi.org/10.1007/s00221-006-0699-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-006-0699-9

Keywords

Navigation