Hippocampus–Prefrontal Coupling Regulates Recognition Memory for Novelty Discrimination

Male 0301 basic medicine 570 hippocampus 1.2 Psychological and socioeconomic processes 1.1 Normal biological development and functioning 150 Prefrontal Cortex 32 Biomedical and Clinical Sciences Prefrontal cortex Basic Behavioral and Social Science Hippocampus context novelty memory Discrimination Learning Rats, Sprague-Dawley 03 medical and health sciences anzsrc-for: 32 Biomedical and Clinical Sciences Memory Behavioral and Social Science Neural Pathways Psychology Animals anzsrc-for: 17 Psychology and Cognitive Sciences 280102 - Expanding knowledge in the biological sciences Neurons prefrontal cortex 0303 health sciences 320903 - Central nervous system Context Neurosciences Novelty Recognition, Psychology 004 Brain Disorders Rats Recognition Mental Health anzsrc-for: 11 Medical and Health Sciences 3209 Neurosciences Neurological anzsrc-for: 3209 Neurosciences Sprague-Dawley recognition
DOI: 10.1523/jneurosci.1202-21.2021 Publication Date: 2021-10-12T21:07:51Z
ABSTRACT
Recognition memory provides the ability to distinguish familiar from novel objects and places, and is important for recording and updating events to guide appropriate behavior. The hippocampus (HPC) and medial prefrontal cortex (mPFC) have both been implicated in recognition memory, but the nature of HPC–mPFC interactions, and its impact on local circuits in mediating this process is not known. Here we show that novelty discrimination is accompanied with higher theta activity (4–10 Hz) and increased c-Fos expression in both these regions. Moreover, theta oscillations were highly coupled between the HPC and mPFC during recognition memory retrieval for novelty discrimination, with the HPC leading the mPFC, but not during initial learning. Principal neurons and interneurons in the mPFC responded more strongly during recognition memory retrieval compared with learning. Optogenetic silencing of HPC input to the mPFC disrupted coupled theta activity between these two structures, as well as the animals' (male Sprague Dawley rats) ability to differentiate novel from familiar objects. These results reveal a key role of monosynaptic connections between the HPC and mPFC in novelty discrimination via theta coupling and identify neural populations that underlie this recognition memory-guided behavior.SIGNIFICANCE STATEMENTMany memory processes are highly dependent on the interregional communication between the HPC and mPFC via neural oscillations. However, how these two brain regions coordinate their oscillatory activity to engage local neural populations to mediate recognition memory for novelty discrimination is poorly understood. This study revealed that the HPC and mPFC theta oscillations and their temporal coupling is correlated with recognition memory-guided behavior. During novel object recognition, the HPC drives mPFC interneurons to effectively reduce the activity of principal neurons. This study provides the first evidence for the requirement of the HPC–mPFC pathway to mediate recognition memory for novelty discrimination and describes a mechanism for how this memory is regulated.
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