Distinct and Dynamic ON and OFF Neural Ensembles in the Prefrontal Cortex Code Social Exploration

Liang, Bo; Zhang, Lifeng; Barbera, Giovanni; Fang, Wenting; Zhang, Jing; Chen, Xiaochun; Chen, Rong; Li, Yun; Lin, Da-Ting

doi:10.1016/j.neuron.2018.08.043

Cited by 124 publications

(140 citation statements)

References 70 publications

Supporting

Mentioning

120

Contrasting

Order By: Relevance

“…We did not see any overall changes in firing rate, only weakly modulated touch and sex-touch neurons at both edges of a zero-centered distribution. While previous rodent studies did not investigate social touch as such, in line with our observations, it has been shown that during social approach (to a caged conspecific) prelimbic responses are weak and diverse 63,64 and that social behaviors are encoded by sparse groups of neurons either increasing or decreasing in activity during behavior ('on' and 'off' ensembles 65 ).…”

Section: Social Touch Responses In Frontal Cortexsupporting

confidence: 87%

Subject sex and partner sex modulate social touch responses across multiple cortical areas

Ebbesen

Bobrov

Rao

et al. 2019

Preprint

View full text Add to dashboard Cite

Touch is a fundamental aspect of social, parental and sexual behavior. Despite our detailed knowledge about cortical processing of non-social touch, we still know little about how social touch cortical circuits. We investigated neural activity across five frontal, motor and sensory cortical areas in rats engaging in naturalistic social facial touch. Information about social touch and the sex of the interaction partner (a biologically significant feature) is a major determinant of cortical activity. 25.3% of units were modulated during social touch and 8.3% of units displayed 'sex-touch' responses (responded differently, depending on the sex of the interaction partner). Single-unit responses were part of a structured, partner-sex-and, in some cases, subject-sex-dependent population response. Simulations suggest that a change in inhibitory drive might underlie these population dynamics. Our observations suggest that socio-sexual characteristics of touch (subject and partner sex) widely modulate cortical activity and need to be investigated with cellular resolution. Single cortical neurons signal social touch and partner sex= 1 = −1 Figure 1 | Diverse cortical responses and variable behavioral timing during social facial touch. (a) The social gap paradigm 27 . Rats separated on two platforms will reach across the gap to engage in social facial touch. In social facial touch, rats align their snouts and whisk to palpate each other's face with their mystacial vibrissae. We recorded the behavior of male and female rats by videography from above in visual darkness under infrared illumination 29,33,34 . (b) Anatomical location of vibrissa motor cortex ('VMC'the primary motor representation of the mystacial vibrissae), cingulate cortex ('ACC'a putative homolog of human/primate anterior cingulate cortex), prelimbic cortex ('PrL'a putative homolog of human/primate medial prefrontal cortex), barrel cortex ('S1'the primary somatosensory representation of the mystacial vibrissae) and auditory cortex ('A1'). (c) Example peri-stimulus time histograms (PSTHs) of touch-activated single neurons (Wilcoxon signed-rank test), aligned to the first whisker-to-whisker touch in each social touch episode. Raster plot above shows single trials, black dots indicate single spikes and vertical line indicates beginning of social facial touch. Black line below indicates mean firing rate, smoothed with an Alpha kernel ( = 75 ms), shaded area indicates s.e.m. (d) Example PSTHs of touch-suppressed single neurons (Wilcoxon signed-rank test), aligned to the first whisker-to-whisker touch in each social touch episode. Same plotting convention as in (c). (e) Top: Histograms of touch duration (red) and inter-touch-time (blue) of social facial touch episodes. The time axes of both plots are clipped at 10 s. Below: Probability distributions of touch duration (red) and inter-touch-interval (blue) of social touch episodes, plotted on a logarithmic time scale. The two distributions span multiple orders of magnitude and strongly overlap.

show abstract

Section: Social Touch Responses In Frontal Cortexsupporting

confidence: 87%

Subject sex and partner sex modulate social touch responses across multiple cortical areas

Ebbesen

Bobrov

Rao

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

“…Thus, imaging approaches can reveal how individual cells embedded in a larger network display coordinated activity during different stages of behavior or training (Wagner et al 2017;Heffley et al 2018;Galiñanes, Bonardi, and Huber 2018;Giovannucci et al 2017) . Moreover, because of their ability to record in freely moving animals, miniscopes have been instrumental in uncovering neural activity patterns occurring during natural behaviors and related brain-states including social interactions (Murugan et al 2017;Remedios et al 2017;Liang et al 2018;Kingsbury et al 2019) or sleep Cox, Pinto, and Dan 2016) with fully intact vestibular input.…”

Section: Introductionmentioning

confidence: 99%

NINscope: a versatile miniscope for multi-region circuit investigations

Groot

Boom

Genderen

et al. 2019

Preprint

View full text Add to dashboard Cite

Miniaturized fluorescence microscopes (miniscopes) have been instrumental to monitor neural activity during unrestrained behavior and their open-source versions have helped to distribute them at an affordable cost. Generally, the footprint and weight of open-source miniscopes is sacrificed for added functionality. Here, we present NINscope: a light-weight, small footprint open-source miniscope that incorporates a high-sensitivity image sensor, an inertial measurement unit (IMU), and an LED driver for an external optogenetic probe. We highlight the advantages of NINscope by performing the first simultaneous cellular resolution (dual scope) recordings from cerebellum and cerebral cortex in unrestrained mice, revealing that the activity of both regions generally precede the onset of behavioral acceleration. At the same time, we demonstrate the optogenetic stimulation capabilities of NINscope and show that cerebral cortical activity can be driven strongly by cerebellar stimulation. Finally, we combine optogenetic stimulation of cortex with imaging in the dorsal striatum and replicate previous studies that show action space is encoded by neurons in this subcortical region. In combination with cross-platform control software NINscope is a versatile addition to the expanding toolbox of open-source miniscopes and will aid multi-region circuit investigations during unrestrained behavior.

show abstract

“…Hippocampus, prefrontal cortex, and context representations. While we present the context-modular memory network as a generic architecture without explicit mention to brain areas and circuits, evidence suggests that contextual signals interact with cortical memories through the hippocampus, prefrontal cortex, and amygdala 1,13,[80][81][82][83][84] . For example, a recent study finds evidence of inhibitory control of cortical memories through the hippocampus 13 , providing direct support for a neuron-specific ( Fig.…”

Section: Circuit Motifs and Cell Types Involved In Gatingmentioning

confidence: 99%

High capacity and dynamic accessibility in associative memory networks with context-dependent neuronal and synaptic gating

Agnes

2020

Preprint

View full text Add to dashboard Cite

Context, such as behavioral state, is known to modulate memory formation and retrieval, but is usually ignored in associative memory models. Here, we propose several types of contextual modulation for associative memory networks that greatly increase their performance. In these networks, context inactivates specific neurons and connections, which modulates the effective connectivity of the network. Memories are stored only by the active components, thereby reducing interference from memories acquired in other contexts. Such networks exhibit several beneficial characteristics, including enhanced memory capacity, high robustness to noise, increased robustness to memory overloading, and better memory retention during continual learning. Furthermore, memories can be biased to have different relative strengths, or even gated on or off, according to contextual cues, providing a candidate model for cognitive control of memory and efficient memory search. An external context-encoding network can dynamically switch the memory network to a desired state, which we liken to experimentally observed contextual signals in prefrontal cortex and hippocampus. Overall, our work illustrates the benefits of organizing memory around context, and provides an important link between behavioral studies of memory and mechanistic details of neural circuits. SIGNIFICANCEMemory is context dependent -both encoding and recall vary in effectiveness and speed depending on factors like location and brain state during a task. We apply this idea to a simple computational model of associative memory through contextual gating of neurons and synaptic connections. Intriguingly, this results in several advantages, including vastly enhanced memory capacity, better robustness, and flexible memory gating. Our model helps to explain (i) how gating and inhibition contribute to memory processes, (ii) how memory access dynamically changes over time, and (iii) how context representations, such as those observed in hippocampus and prefrontal cortex, may interact with and control memory processes.FIG. 1. Schematic of the context-modular memory network. A, Associative memory is defined hierarchically through a set of contexts (c 1 to c 5 ) and memory patterns (m 1 to m 15 ) assigned to each one. B, Network implementation: neurons are arranged into contextual configurations (subnetworks) in two ways: neuron-specific gating, where context is defined as a proportion of available neurons (colored rings; defined randomly, spatial localization is illustrative), and synapse-specific gating, where context is defined as a proportion of gated synapses (red cross, bottom right inset). Context is controlled by an external contextencoding network, such that one context is active at a time (black ring), and memories outside of the active context remain dormant. C, Contextual configurations change the effective connectivity matrix of the associative memory network: neuron-specific gating removes particular columns and rows (left), synapse-specific gating removes individual elemen...

show abstract

Distinct and Dynamic ON and OFF Neural Ensembles in the Prefrontal Cortex Code Social Exploration

Cited by 124 publications

References 70 publications

Subject sex and partner sex modulate social touch responses across multiple cortical areas

Subject sex and partner sex modulate social touch responses across multiple cortical areas

NINscope: a versatile miniscope for multi-region circuit investigations

High capacity and dynamic accessibility in associative memory networks with context-dependent neuronal and synaptic gating

Contact Info

Product

Resources

About