Combined Social and Spatial Coding in a Descending Projection from the Prefrontal Cortex

Murugan, Malavika; Jang, Hee Jae; Park, Michelle; Miller, Ellia M.; Cox, Julia; Taliaferro, Joshua P; Parker, Nathan F.; Bhave, Varun; Hur, Hong; Liang, Yupu; Nectow, Alexander R.; Pillow, Jonathan W.; Witten, Ilana B.

doi:10.1016/j.cell.2017.11.002

Cited by 270 publications

(237 citation statements)

References 54 publications

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“…2e; ANOVA, all p ’s > 0.05). However, projections to VS were significantly more pronounced than to BLA for both PL ( F (1, 60) = 24.87, p < 0.001) and IL ( F (1, 61) = 18.86, p < 0.001), consistent with anatomical studies (Gabbott et al 2005; Murugan et al 2017). PL neurons projecting to BLA were located mainly in superficial layers, whereas VS projecting neurons were located mainly in deeper layers, consistent with recent studies (Cheriyan et al 2016; Gabbott et al 2005; Murugan et al 2017).…”

Section: Resultssupporting

confidence: 87%

Prefrontal circuits signaling active avoidance retrieval and extinction

et al. 2018

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Objective Neurons in PL and IL project densely to two areas implicated in active avoidance: the basolateral amygdala (BLA) and the ventral striatum (VS). We therefore combined c-Fos immunohistochemistry with retrograde tracers to characterize signaling in platform-mediated active avoidance. Methods Male rats were infused with retrograde tracers (CTB, FB) into basolateral amygdala and ventral striatum and conditioned to avoid tone-signaled footshocks by stepping onto a nearby platform. In a subsequent test session, rats received either 2 unreinforced tones (avoidance retrieval) or 15 unreinforced tones (avoidance extinction) followed by analysis of c-Fos combined with fluorescent imaging of retrograde tracers. Results Retrieval of avoidance did not activate IL neurons, but did activate PL neurons projecting to BLA, and to a lesser extent VS. Extinction of avoidance activated IL neurons projecting to both BLA and VS, as well as PL neurons projecting to VS. Conclusions Our observation that avoidance retrieval is signaled by PL projections to BLA suggests that PL may modulate VS indirectly via BLA, and agrees with other findings implicating BLA in active avoidance. Less expected was the signaling of extinction via PL inputs to VS, which may converge with IL inputs to VS to inhibit expression of avoidance.

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Section: Resultssupporting

confidence: 87%

Prefrontal circuits signaling active avoidance retrieval and extinction

et al. 2018

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“…This highlights the importance of studying activity preceding initiation of behavior, which may shed light on circuits that can regulate downstream mechanisms to influence behavior. This pre "active" increase in dmPFC-PVI activity may be important for gating specific projection neurons while inhibiting specific "anti-social" subcortical projections from dmPFC [37][38][39] , leading to selective activation of circuits necessary for subsequent social interaction. Alternatively, given that brief optogenetic modulation of dmPFC-PVI at gamma frequency triggers active social approach, rhythmic dmPFC activity in the gamma oscillation range may be necessary for expression of normal social approach, as it is for attentional behavior, without impacting the overall excitation of dmPFC region ( Supplementary Fig.…”

Section: Discussionmentioning

confidence: 99%

Prefrontal parvalbumin interneurons require juvenile social experience to establish adult social behavior

et al. 2020

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Social isolation during the juvenile critical window is detrimental to proper functioning of the prefrontal cortex (PFC) and establishment of appropriate adult social behaviors. However, the specific circuits that undergo social experience-dependent maturation to regulate social behavior are poorly understood. We identify a specific activation pattern of parvalbuminpositive interneurons (PVIs) in dorsal-medial PFC (dmPFC) prior to an active bout, or a bout initiated by the focal mouse, but not during a passive bout when mice are explored by a stimulus mouse. Optogenetic and chemogenetic manipulation reveals that brief dmPFC-PVI activation triggers an active social approach to promote sociability. Juvenile social isolation decouples dmPFC-PVI activation from subsequent active social approach by freezing the functional maturation process of dmPFC-PVIs during the juvenile-to-adult transition. Chemogenetic activation of dmPFC-PVI activity in the adult animal mitigates juvenile isolationinduced social deficits. Therefore, social experience-dependent maturation of dmPFC-PVI is linked to long-term impacts on social behavior.

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“…In contrast, at the few responsive sites in superficial layers we observed almost exclusively 22 kHz evoked calls, which are associated with fear or negative effect. Interestingly, superficial layers are known to project to the amygdala, whereas deep layers project to the ventral tegmental area (Murugan et al., ). It is tempting to speculate that the generation of 22 kHz calls is at least partly mediated by amygdala projecting prelimbic neurons, whereas the generation of 50 kHz calls might be facilitated by ventral tegmental area projecting prelimbic neurons.…”

Section: Discussionmentioning

confidence: 99%

Involvement of rat posterior prelimbic and cingulate area 2 in vocalization control

Bennett

Maier

Brecht

2019

Eur J of Neuroscience

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Microstimulation mapping identified vocalization areas in primate anterior cingulate cortex. Rat anterior cingulate and medial prefrontal areas have also been intensely investigated, but we do not know, how these cortical areas contribute to vocalizations and no systematic mapping of stimulation‐evoked vocalizations has been performed. To address this question, we mapped microstimulation‐evoked (ultrasonic) vocalizations in rat cingulate and medial prefrontal cortex. The incidence of evoked vocalizations differed markedly between frontal cortical areas. Vocalizations were most often evoked in posterior prelimbic cortex and cingulate area 2, whereas vocalizations were rarely evoked in dorsal areas (vibrissa motor cortex, secondary motor cortex and cingulate area 1) and anterior areas (anterior prelimbic, medial‐/ventral‐orbital cortex). Vocalizations were observed at intermediate frequencies in ventro‐medial areas (infralimbic and dorsopeduncular cortex). Various complete, naturally occurring calls could be elicited. In prelimbic cortex superficial layer microstimulation evoked mainly fear calls with low efficacy, whereas deep layer microstimulation evoked mainly 50 kHz calls with high efficacy. Vocalization stimulation thresholds were substantial (70–500 μA, the maximum tested; on average ~400 μA) and latencies were long (median 175 ms). Posterior prelimbic cortex projected to numerous targets and innervated brainstem vocalization centers such as the intermediate reticular formation and the nucleus retroambiguus disynaptically via the periaqueductal gray. Anatomical position, stimulation effects and projection targets of posterior prelimbic cortex were similar to that of monkey anterior cingulate vocalization cortex. Our data suggest that posterior prelimbic cortex is more closely involved in control of vocalization initiation than in specifying acoustic details of vocalizations.

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Combined Social and Spatial Coding in a Descending Projection from the Prefrontal Cortex

Cited by 270 publications

References 54 publications

Prefrontal circuits signaling active avoidance retrieval and extinction

Prefrontal circuits signaling active avoidance retrieval and extinction

Prefrontal parvalbumin interneurons require juvenile social experience to establish adult social behavior

Involvement of rat posterior prelimbic and cingulate area 2 in vocalization control

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