Abstract
Prefrontal cortical GABAergic interneurons (INs) and their innervations are essential for the execution of complex behaviors such as working memory, social behavior, and fear expression. These behavior regulations are highly dependent on primary long-range afferents originating from the subcortical structures such as mediodorsal thalamus (MD), ventral hippocampus (vHPC), and basolateral amygdala (BLA). In turn, the regulatory effects of these inputs are mediated by activation of parvalbumin-expressing (PV) and/or somatostatin expressing (SST) INs within the prefrontal cortex (PFC). Here we review how each of these long-range afferents from the MD, vHPC, or BLA recruits a subset of the prefrontal interneuron population to exert precise control of specific PFC-dependent behaviors. Specifically, we first summarize the anatomical connections of different long-range inputs formed on prefrontal GABAergic INs, focusing on PV versus SST cells. Next, we elaborate on the role of prefrontal PV- and SST- INs in regulating MD afferents-mediated cognitive behaviors. We also examine how prefrontal PV- and SST- INs gate vHPC afferents in spatial working memory and fear expression. Finally, we discuss the possibility that prefrontal PV-INs mediate fear conditioning, predominantly driven by the BLA-mPFC pathway. This review will provide a broad view of how multiple long-range inputs converge on prefrontal interneurons to regulate complex behaviors and novel future directions to understand how PFC controls different behaviors.
Highlights
The prefrontal cortex (PFC) is well known for its topdown control of multiple distinct complex behaviors, including cognitive, emotional, and social behaviors, by selectively processing different input information (Carmichael and Price, 1996; Amodio and Frith, 2006; Hoover and Vertes, 2007; Yizhar and Levy, 2021)
This study provides a piece of direct evidence for the role of MDmPFC pathway in cognitive function
Prefrontal pyramidal neuron activity features sequential firing during the delay period of working memory tasks (Bolkan et al, 2017; Schmitt et al, 2017). These pyramidal neurons’ sequential activity probably depends on both mediodorsal thalamus (MD) afferents and PV-INs driving feedforward inhibition. Both PV- and somatostatin expressing (SST)-INs display high firing rates during the delay period of the working memory task (Kim et al, 2016), no study has been done to explore whether the activity of SST-INs in the medial PFC (mPFC) is driven by MD inputs while performing the task
Summary
The prefrontal cortex (PFC) is well known for its topdown control of multiple distinct complex behaviors, including cognitive, emotional, and social behaviors, by selectively processing different input information (Carmichael and Price, 1996; Amodio and Frith, 2006; Hoover and Vertes, 2007; Yizhar and Levy, 2021). Often overlooked in the literature, vHPC afferents form excitatory synapses on pyramidal neurons and INs to promote feedforward inhibition (Figure 1B) (Thierry et al, 2000; Gabbott et al, 2002; Dégenètais et al, 2003; Dembrow et al, 2015; Liu and Carter, 2018; Marek et al, 2018) These inputs synapse on both PV- and SST- INs in the mPFC, and stimulation of vHPC inputs successfully induces EPSCs on both excitatory and inhibitory cells (Abbas et al, 2018; Phillips et al, 2019). McGarry and Carter (2016) reported that BLA inputs synapsed on cortico-amygdalar excitatory neurons but formed stronger connections with nearby PVand SST- INs. activating BLA inhibits most pyramidal neurons in the mPFC by activating PV-INs (Floresco and Tse, 2007; Dilgen et al, 2013), indicating a powerful inhibitory control of the prefrontal network activity by the BLA. DISTINCT ROLES OF THREE LONG-RANGE AFFERENTS IN THE MPFC IN REGULATING COMPLEX BEHAVIOR
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