Evidence for two distinct thalamocortical circuits in retrosplenial cortex

Lomi, E., Mathiasen, M. L., Cheng, H. Y., Zhang, N., Aggleton, J. P., Mitchell, A. S. and Jeffery, K. J. (2021) Evidence for two distinct thalamocortical circuits in retrosplenial cortex. Neurobiology of Learning and Memory, 185, 107525. (doi: 10.1016/j.nlm.2021.107525) (PMID:34555510)

Abstract

Retrosplenial cortex (RSC) lies at the interface between sensory and cognitive networks in the brain and mediates between these, although it is not yet known how. It has two distinct subregions, granular (gRSC) and dysgranular (dRSC). The present study investigated how these subregions differ with respect to their electrophysiology and thalamic connectivity, as a step towards understanding their functions. The gRSC is more closely connected to the hippocampal formation, in which theta-band local field potential oscillations are prominent. We, therefore, compared theta-rhythmic single-unit activity between the two RSC subregions and found, mostly in gRSC, a subpopulation of non-directional cells with spiking activity strongly entrained by theta oscillations, suggesting a stronger coupling of gRSC to the hippocampal system. We then used retrograde tracers to test for differential inputs to RSC from the anteroventral thalamus (AV). We found that gRSC and dRSC differ in their afferents from two AV subfields: dorsomedial (AVDM) and ventrolateral (AVVL). Specifically: (1) as a whole AV projects more strongly to gRSC; (2) AVVL targets both gRSC and dRSC, while AVDM provides a selective projection to gRSC, (3) the gRSC projection is layer-specific: AVDM targets specifically gRSC superficial layers. These same AV projections are topographically organized with ventral AV neurons innervating rostral RSC and dorsal AV neurons innervating caudal RSC. These combined results suggest the existence of two distinct but interacting RSC subcircuits: one connecting AVDM to gRSC that may comprise part of the cognitive hippocampal system, and the other connecting AVVL to both RSC regions that may link hippocampal and perceptual regions. We suggest that these subcircuits are distinct to allow for differential weighting during integration of converging sensory and cognitive computations: an integration that may take place in thalamus, RSC, or both.

• Item Type: Articles
• Additional Information: KJ was supported by grants from Wellcome (103896AIA) and the Royal Society (IEC\R2\181140). ASM was supported by a Wellcome Trust Senior Research Fellowship (WT 110157/Z/15/Z). JPA and MM were supported by grants from Wellcome (103722/Z14/Z) and the UK BBSRC (BB/T007249/1). EL was supported by a Medical Sciences Division Graduate School Studentship, University of Oxford: Clarendon Fund – Department of Experimental Psychology –Somerville College Mary Somerville Graduate Studentship (SFF1718_CB2_ MSD_1074636). H.Y.C. was supported by the National Science Scholarship (PhD) from the A*Star Graduate Academy. N.Z. was supported by a scholarship from the China Scholarship Council (201608000007).
• Status: Published
• Refereed: Yes
• Glasgow Author(s) Enlighten ID: Jeffery, Professor Kate

Creator Roles

Jeffery, K. J.: Conceptualization, Funding acquisition, Methodology, Project administration, Resources, Supervision, Validation, Writing – original draft, Writing – review and editing

• Authors: Lomi, E., Mathiasen, M. L., Cheng, H. Y., Zhang, N., Aggleton, J. P., Mitchell, A. S., and Jeffery, K. J.
• College/School: College of Medical Veterinary and Life Sciences > School of Psychology & Neuroscience
• Journal Name: Neurobiology of Learning and Memory
• Publisher: Elsevier
• ISSN: 1074-7427
• ISSN (Online): 1095-9564
• Published Online: 20 September 2021