Disconnection of the Perirhinal and Postrhinal Cortices Impairs Recognition of Objects in Context But Not Contextual Fear Conditioning

Abstract

The perirhinal cortex (PER) is known to process object information, whereas the rodent postrhinal cortex (POR), homolog to the parahippocampal cortex in primates, is thought to process spatial information. A number of studies, however, provide evidence that both areas are involved in processing contextual information. In this study, we tested the hypothesis that the rat POR relies on object information received from the PER to form complex representations of context. Using three fear-conditioning (FC) paradigms (signaled, unsignaled, and renewal) and two context-guided object recognition tasks (with 3D and 2D objects), we examined the effects of crossed excitotoxic lesions to the POR and the contralateral PER. Performance of rats with crossed lesions was compared with that of rats with ipsilateral POR plus PER lesions and sham-operated rats. We found that rats with contralateral PER-POR lesions were impaired in object-context recognition but not in contextual FC. Therefore, interaction between the POR and PER is necessary for context-guided exploratory behavior but not for associating fear with context. Our results provide evidence for the hypothesis that the POR relies on object and pattern information from the PER to encode representations of context. The association of fear with a context, however, may be supported by alternate cortical and/or subcortical pathways when PER-POR interaction is not available. Our results suggest that contextual FC may represent a special case of context-guided behavior. Representations of context are important for perception, memory, decision making, and other cognitive processes. Moreover, there is extensive evidence that the use of contextual representations to guide appropriate behavior is disrupted in neuropsychiatric and neurological disorders including developmental disorders, schizophrenia, affective disorders, and Alzheimer's disease. Many of these disorders are accompanied by changes in parahippocampal and hippocampal structures. Understanding how context is represented in the brain and how parahippocampal structures are involved will enhance our understanding and treatment of the cognitive and behavioral symptoms associated with neurological disorders and neuropsychiatric disease.

CA1-projecting subiculum neurons facilitate object–place learning

“…Efferents of the CA1-projecting SUB neurons also target perirhinal cortex ( Fig. 1i-l), an area strongly implicated in object-place learning 15 .…”

“…In light of our circuit mapping results, it is clear that visual and retrosplenial cortical input can reach perirhinal cortex through direct projections from CA1-projecting SUB neurons. Like CA1, perirhinal cortex neurons respond to objects 42,45 and lesions produce impairments in expression of object-place memory 15,46 . Beta-frequency and gammafrequency paced stimulation of perirhinal cortex bi-directionally modulates recognition of objects as familiar versus novel 47 .…”

Interactions between stimulus and response types are more strongly represented in the entorhinal cortex than in its upstream regions in rats

“…Visual scenes used in our tasks may be considered as a context, and the PER-POR networks may play significant roles in contextual object recognition ( Norman and Eacott, 2005 ; Heimer-McGinn et al, 2017 ). In natural situations, an animal never experiences an object completely detached from its background, and a visual context also always involves objects in it ( Aminoff et al, 2013 ).…”

Involvement of the Postrhinal and Perirhinal Cortices in Microscale and Macroscale Visuospatial Information Encoding

“…According to this hypothesis, spatial information is processed in the POR and sent to the hippocampus via the medial entorhinal cortex (MEC), whereas non-spatial information is processed by the PRC via the lateral entorhinal cortex (LEC) before the hippocampus is involved (Burwell et al, 1995(Burwell et al, , 2004Burwell and Amaral, 1998b;Eichenbaum and Lipton, 2008). More recent studies suggest, however, that the functions of the parahippocampal regions do not strictly align to the two-streams hypothesis: both the POR and PRC are involved in different kinds of spatial and non-spatial information processing (Brown and Aggleton, 2001;Ramos, 2002Ramos, , 2008Ramos, , 2013aRamos, ,b, 2017Burwell et al, 2004;Winters et al, 2004;Ramos and Vaquero, 2005;Furtak et al, 2012;Heimer-McGinn et al, 2017;Ramos, 2017;Burke et al, 2018;LaChance et al, 2019).…”