T-type calcium channels cause bursts of spikes in motor but not sensory thalamic neurons during mimicry of natural patterns of synaptic input

Kim, Haram; Hong, Su Z.; Fiorillo, Christopher D.

doi:10.3389/fncel.2015.00428

Cited by 8 publications

(7 citation statements)

References 87 publications

(174 reference statements)

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“…4g). MD neurons in vitro have a bimodal resting membrane potential distribution 37 , suggesting different degrees of excitability. Because our analysis suggested that two MD populations are driven by different degrees of cortical engagement ( Supplementary Fig.…”

Section: Neurons Regulate Pfc Representational Switching Likely Thmentioning

confidence: 99%

Thalamic regulation of switching between cortical representations enables cognitive flexibility

2018

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Interactions between the prefrontal cortex (PFC) and mediodorsal thalamus (MD) are critical for cognitive flexibility, yet the underlying computations are unknown. To investigate fronto-thalamic substrates of cognitive flexibility, we developed a behavioral task, where mice switched between different sets of learned cues that guided attention towards either visual or auditory targets. We found that PFC responses reflected both the individual cues and their meaning as task rules, indicating a hierarchical cue-to-rule transformation. Conversely, MD responses reflected the statistical regularity of cue presentation, and were required for switching between such experimentally-specified cueing contexts. A subset of these thalamic responses sustained contextrelevant PFC representations, while another suppressed the context-irrelevant ones. Through modeling and experimental validation, we find that thalamic-mediated suppression may not only reduce PFC representational interference but could also preserve unused cortical traces for future use. Overall, our study provides a computational foundation for thalamic engagement in cognitive flexibility. Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:

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Section: Neurons Regulate Pfc Representational Switching Likely Thmentioning

confidence: 99%

Thalamic regulation of switching between cortical representations enables cognitive flexibility

2018

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“…Adaptation had a more striking effect on burst firing and synchronous evoked spikes. Bursts -groups of spikes with very short inter-spike intervals made possible by the de-inactivation of T-type calcium channels (Kim et al, 2015;S. Suzuki & Rogawski, 1989) -have been shown to provide potent synaptic drive to S1 (Sherman, 2001;Swadlow, 2002;Swadlow & Gusev, 2001), and may therefore be critical for shaping cortical sensory responses.…”

Section: Adaptation Primarily Influences Feature Response Timing In Vmentioning

confidence: 99%

Rapid Cortical Adaptation and the Role of Thalamic Synchrony During Wakefulness

Borden

Liew

et al. 2020

Preprint

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Rapid sensory adaptation is observed across all sensory systems, and strongly shapes sensory percepts in complex sensory environments. Yet despite its ubiquity and likely necessity for survival, the mechanistic basis is poorly understood. A wide range of studies primarily in in-vitro and anesthetized preparations have pointed to the emergence of adaptation effects at the level of primary sensory cortex, with only modest signatures in earlier stages of processing. The nature of rapid adaptation and how it shapes sensory representations during wakefulness, and thus the potential role in adaptive changes in perception, is unknown, as are the mechanisms that underlie this phenomenon. To address these unknowns, we recorded spiking activity in primary somatosensory cortex (S1) and the upstream ventral posteromedial (VPm) thalamic nucleus in the vibrissa pathway of the awake mouse, and quantified responses to whisker stimuli delivered in isolation and embedded in an adapting sensory background. We found that during wakefulness, cortical sensory responses were indeed adapted by persistent sensory stimulation; putative excitatory neurons were profoundly adapted, and inhibitory neurons only modestly so. Further optogenetic manipulation experiments and network modeling suggest this largely reflects adaptive changes in synchronous thalamic firing combined with robust engagement of feedforward inhibition, with little contribution from synaptic depression. Taken together, these results suggest that cortical adaptation largely reflects changes in timing of thalamic input, and the way in which this differentially impacts cortical excitation and feedforward inhibition, pointing to a prominent role of thalamic gating in rapid adaptation of primary sensory cortex.Significance StatementRapid adaptation of sensory activity strongly shapes representations of sensory inputs across all sensory pathways over the timescale of seconds, and has profound effects on sensory perception. Despite its ubiquity and theoretical role in the efficient encoding of complex sensory environments, the mechanistic basis is poorly understood, particularly during wakefulness. In this study in the vibrissa pathway of awake mice, we show that cortical representations of sensory inputs are strongly shaped by rapid adaptation, and that this is mediated primarily by adaptive gating of the thalamic inputs to primary sensory cortex and the differential way in which these inputs engage cortical sub-populations of neurons.

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“…For example, the theory correctly predicted the experimental observation that T-type calcium channels are homoeostatic in counterbalancing opponent IPSG in thalamocortical neurons of LGN 50 . The more general theory proposes differences between sensory and motor neurons, and it correctly predicted evidence that T-type calcium channels are not homoeostatic but cause bursts of spikes in motor thalamus 51 . In addition to predicting the properties of a type of neuron, theory may also be useful in explaining variability in ion channel parameters across neurons of the same type, particularly by indicating which combinations of ion channel parameters work in a concerted manner to maintain near optimal homoeostatic excitability 60 61 .…”

Section: Discussionmentioning

confidence: 84%

“…Together with recent experiments 50 51 , we have tested a theory of the information contributed to membrane voltage by synapses and ion channels 21 40 52 53 . The theory extends a long line of research relating neuronal function to quantitative principles of information 23 24 .…”

Section: Discussionmentioning

confidence: 99%

Theory of optimal balance predicts and explains the amplitude and decay time of synaptic inhibition

Kim

Fiorillo

2017

Nat Commun

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Synaptic inhibition counterbalances excitation, but it is not known what constitutes optimal inhibition. We previously proposed that perfect balance is achieved when the peak of an excitatory postsynaptic potential (EPSP) is exactly at spike threshold, so that the slightest variation in excitation determines whether a spike is generated. Using simulations, we show that the optimal inhibitory postsynaptic conductance (IPSG) increases in amplitude and decay rate as synaptic excitation increases from 1 to 800 Hz. As further proposed by theory, we show that optimal IPSG parameters can be learned through anti-Hebbian rules. Finally, we compare our theoretical optima to published experimental data from 21 types of neurons, in which rates of synaptic excitation and IPSG decay times vary by factors of about 100 (5-600 Hz) and 50 (1-50 ms), respectively. From an infinite range of possible decay times, theory predicted experimental decay times within less than a factor of 2. Across a distinct set of 15 types of neuron recorded in vivo, theory predicted the amplitude of synaptic inhibition within a factor of 1.7. Thus, the theory can explain biophysical quantities from first principles.

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T-type calcium channels cause bursts of spikes in motor but not sensory thalamic neurons during mimicry of natural patterns of synaptic input

Cited by 8 publications

References 87 publications

Thalamic regulation of switching between cortical representations enables cognitive flexibility

Thalamic regulation of switching between cortical representations enables cognitive flexibility

Rapid Cortical Adaptation and the Role of Thalamic Synchrony During Wakefulness

Theory of optimal balance predicts and explains the amplitude and decay time of synaptic inhibition

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