Perirhinal and Postrhinal Contributions to Remote Memory for Context

The perirhinal (PER) and postrhinal (POR) cortices, two components of the medial temporal lobe memory system, are reciprocally connected with the hippocampus both directly and via the entorhinal cortex. Damage to PER or POR before or shortly after training on a contextual fear conditioning task causes deficits in the subsequent expression of contextual fear, implicating these regions in the acquisition or expression of contextual memory. Here, we examined the contribution of PER and POR to the processing of remotely learned contextual information. Male Long-Evans rats were trained in an unsignaled contextual fear conditioning paradigm. After training, rats received bilateral neurotoxic lesions to PER or POR or sham control surgeries at three different training-to-lesion intervals: 1, 28, or 100 d after training. Two weeks after surgery, lesioned and control rats were returned to the training context to assess contextual fear as measured by freezing. Rats with PER or POR damage froze significantly less in the training context than control rats but were not different from each other. The severity of the deficit did not differ across training-to-lesion intervals for any group. This pattern of deficits differs from that of posttraining hippocampal lesions, for which longer training-to-lesion intervals produce significantly more fear-conditioned contextual freezing than shorter training-to-lesion intervals. In the absence of such a retrograde gradient in the present study, our interpretation is that PER and POR have an ongoing role in the storage or retrieval of representations for context. Alternatively, these regions may be involved in a more extended consolidation process that becomes apparent beyond 100 d after learning.

[1]  L. Nadel,et al.  Context and conditioning: A place for space , 1980 .

[2]  M. Fanselow,et al.  Conditional and unconditional components of post-shock freezing , 1980, The Pavlovian journal of biological science.

[3]  G. V. Hoesen,et al.  A direct projection from the perirhinal cortex (area 35) to the subiculum in the rat , 1983, Brain Research.

[4]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[5]  J N Rawlins,et al.  The hippocampus and conditioning to contextual cues. , 1987, Behavioral neuroscience.

[6]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[7]  M. Fanselow,et al.  Modality-specific retrograde amnesia of fear. , 1992, Science.

[8]  M. Davis,et al.  Lesions of the perirhinal cortex but not of the frontal, medial prefrontal, visual, or insular cortex block fear-potentiated startle using a visual conditioned stimulus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  H. Eichenbaum,et al.  Two functional components of the hippocampal memory system , 1994, Behavioral and Brain Sciences.

[10]  Joseph E LeDoux,et al.  Disruptive effects of posttraining perirhinal cortex lesions on conditioned fear: contributions of contextual cues. , 1995, Behavioral neuroscience.

[11]  James L. McClelland,et al.  Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. , 1995, Psychological review.

[12]  L N Cooper,et al.  Temporally graded retrograde amnesia following separate and combined lesions of the perirhinal cortex and fornix in the rat. , 1996, Learning & memory.

[13]  Memory: Old questions, new perspectives , 1997, Current Biology.

[14]  M. Fanselow,et al.  Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats , 1997, Behavioural Brain Research.

[15]  M. Witter,et al.  Parallel input to the hippocampal memory system through peri‐ and postrhinal cortices , 1997, Neuroreport.

[16]  T. Otto,et al.  Odor-guided fear conditioning in rats: 2. Lesions of the anterior perirhinal cortex disrupt fear conditioned to the explicit conditioned stimulus but not to the training context. , 1997, Behavioral neuroscience.

[17]  M. Cassell,et al.  Cortical, thalamic, and amygdaloid projections of rat temporal cortex , 1997, The Journal of comparative neurology.

[18]  D. Amaral,et al.  Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat , 1998 .

[19]  The startled seahorse: Is the hippocampus necessary for contextual fear conditioning? , 1998 .

[20]  D. Amaral,et al.  Perirhinal and postrhinal cortices of the rat: Interconnectivity and connections with the entorhinal cortex , 1998, The Journal of comparative neurology.

[21]  M. W. Brown,et al.  Episodic memory, amnesia, and the hippocampal–anterior thalamic axis , 1999, Behavioral and Brain Sciences.

[22]  P. Holland,et al.  Hippocampus and context in classical conditioning , 1999, Current Opinion in Neurobiology.

[23]  M. Fanselow,et al.  Temporally Graded Retrograde Amnesia of Contextual Fear after Hippocampal Damage in Rats: Within-Subjects Examination , 1999, The Journal of Neuroscience.

[24]  C Bucherelli,et al.  Auditory Thalamus, Dorsal Hippocampus, Basolateral Amygdala, and Perirhinal Cortex Role in the Consolidation of Conditioned Freezing to Context and to Acoustic Conditioned Stimulus in the Rat , 1999, The Journal of Neuroscience.

[25]  E. Maguire,et al.  Patterns of hippocampal‐cortical interaction dissociate temporal lobe memory subsystems , 2000, Hippocampus.

[26]  D. Mumby,et al.  Anterograde and retrograde memory for object discriminations and places in rats with perirhinal cortex lesions , 2000, Behavioural Brain Research.

[27]  R G Phillips,et al.  Contributions of postrhinal and perirhinal cortex to contextual information processing. , 2000, Behavioral neuroscience.

[28]  T. Bussey,et al.  Consolidation and the medial temporal lobe revisited: Methodological considerations † , 2001, Hippocampus.

[29]  R. Sutherland,et al.  Retrograde amnesia after hippocampal damage: Recent vs. remote memories in two tasks , 2001, Hippocampus.

[30]  L. Nadel,et al.  Consolidation of memory , 2001, Hippocampus.

[31]  L. Nadel,et al.  The hippocampal complex and long-term memory revisited , 2001, Trends in Cognitive Sciences.

[32]  L R Squire,et al.  Retrograde amnesia † , 2001, Hippocampus.

[33]  L. Jarrard,et al.  Retrograde amnesia and consolidation: Anatomical and lesion considerations , 2001, Hippocampus.

[34]  M Moscovitch,et al.  Anterograde and retrograde amnesia in rats with large hippocampal lesions , 2001, Hippocampus.

[35]  Greg D. Gale,et al.  Hippocampus and contextual fear conditioning: Recent controversies and advances , 2001, Hippocampus.

[36]  E. Baldi,et al.  Differential contribution of some cortical sites to the formation of memory traces supporting fear conditioning , 2002, Experimental Brain Research.

[37]  D. Bucci,et al.  Contextual fear discrimination is impaired by damage to the postrhinal or perirhinal cortex. , 2002, Behavioral neuroscience.

[38]  Contextual fear discrimination is impaired by damage to the postrhinal or perirhinal cortex. , 2002 .

[39]  D. Mumby,et al.  Perirhinal cortex lesions produce variable patterns of retrograde amnesia in rats , 2003, Behavioural Brain Research.

[40]  Derick H. Lindquist,et al.  Perirhinal Cortex Supports Delay Fear Conditioning to Rat Ultrasonic Social Signals , 2004, The Journal of Neuroscience.

[41]  M. Baxter,et al.  Preserved anterograde and retrograde memory of rapidly acquired olfactory discrminations after neurotoxic hippocampal lesions , 2004, Hippocampus.

[42]  Rebecca D Burwell,et al.  Corticohippocampal Contributions to Spatial and Contextual Learning , 2004, The Journal of Neuroscience.

[43]  H. Schnitzler,et al.  Temporary inactivation of the perirhinal cortex by muscimol injections block acquisition and expression of fear‐potentiated startle , 2004, The European journal of neuroscience.

[44]  D. Bucci,et al.  Deficits in attentional orienting following damage to the perirhinal or postrhinal cortices. , 2004, Behavioral neuroscience.