Modular Network between Postrhinal Visual Cortex, Amygdala, and Entorhinal Cortex

The postrhinal area (POR) is a known center for integrating spatial with nonspatial visual information and a possible hub for influencing landmark navigation by affective input from the amygdala. This may involve specific circuits within muscarinic acetylcholine receptor 2 (M2)-positive (M2⁺) or M2^- modules of POR that associate inputs from the thalamus, cortex, and amygdala, and send outputs to the entorhinal cortex. Using anterograde and retrograde labeling with conventional and viral tracers in male and female mice, we found that all higher visual areas of the ventral cortical stream project to the amygdala, while such inputs are absent from primary visual cortex and dorsal stream areas. Unexpectedly for the presumed salt-and-pepper organization of mouse extrastriate cortex, tracing results show that inputs from the dorsal lateral geniculate nucleus and lateral posterior nucleus were spatially clustered in layer 1 (L1) and overlapped with M2⁺ patches of POR. In contrast, input from the amygdala to L1 of POR terminated in M2^- interpatches. Importantly, the amygdalocortical input to M2^- interpatches in L1 overlapped preferentially with spatially clustered apical dendrites of POR neurons projecting to amygdala and entorhinal area lateral, medial (ENTm). The results suggest that subnetworks in POR, used to build spatial maps for navigation, do not receive direct thalamocortical M2⁺ patch-targeting inputs. Instead, they involve local networks of M2^- interpatches, which are influenced by affective information from the amygdala and project to ENTm, whose cells respond to visual landmark cues for navigation.SIGNIFICANCE STATEMENT A central purpose of visual object recognition is identifying the salience of objects and approaching or avoiding them. However, it is not currently known how the visual cortex integrates the multiple streams of information, including affective and navigational cues, which are required to accomplish this task. We find that in a higher visual area, the postrhinal cortex, the cortical sheet is divided into interdigitating modules receiving distinct inputs from visual and emotion-related sources. One of these modules is preferentially connected with the amygdala and provides outputs to entorhinal cortex, constituting a processing stream that may assign emotional salience to objects and landmarks for the guidance of goal-directed navigation.