Flexible Sensory Representations in Auditory Cortex Driven by Behavioral Relevance

Kato, Hiroyuki; Gillet, Shea N.; Isaacson, Jeffry S.

doi:10.1016/j.neuron.2015.10.024

Cited by 231 publications

(322 citation statements)

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“…Taken together, data from insect and mammalian nervous systems suggest that habituation may generally arise through the formation of inhibitory engrams created via inhibitory synaptic potentiation (6,7,9,10,13). We note that in the mammalian brain, the subtypes of inhibitory interneurons involved and their mode of regulation may depend on the particular neural circuit in which they are embedded.…”

Section: Negative Images In Adaptive Stimulus Filtering and Behavioramentioning

confidence: 71%

“…Although mechanisms for memory recall could vary across brain systems and circuits, we suggest neocortical disinhibition as one potential strategy to allow release of strongly connected excitatory ensembles from balanced strong inhibition (13,39,41). Thus, in addition to the established function of local disinhibition to enhance excitatory transmission (18) and initial encoding of memory (12,20,21), disinhibition may play a significant role in facilitating release and recall of previously learned but latent cortical associations (11).…”

Section: Inhibitory Engrams In Associative Memory Storage and Recallmentioning

confidence: 91%

“…Habituation can thus be characterized as a 10-fold reduction in the excitation/inhibition ratio of population activity. Interestingly, when attention to the tone becomes important for task performance, SOM inhibition is reduced and pyramidal cell responses to the tone increase even in habituated animals (13).…”

Section: Negative Images In Adaptive Stimulus Filtering and Behavioramentioning

confidence: 99%

“…Although the precise interaction between these different subtypes is not yet clear, the model in which matched inhibition drives habituation generates important predictions. One notable corollary suggests that innate behavioral responses attenuated by habituation can later be rapidly restored through disinhibition, via inputs that silence the relevant inhibitory neurons (13).…”

Section: Negative Images In Adaptive Stimulus Filtering and Behavioramentioning

confidence: 99%

“…Here, we discuss how these inhibitory engrams created through compensatory inhibitory potentiation contribute to cognitive function, and ask how their disturbance could contribute to clinical features and transdiagnostic traits observed in neuropsychiatric conditions. In doing so, we integrate insights from diverse neurophysiological, behavioral, computational, and brain imaging studies across multiple species to extract and highlight fundamental principles of memory consolidation and recall (7,8,(10)(11)(12)(13).…”

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confidence: 99%

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Inhibitory engrams in perception and memory

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Vogels

Behrens

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

135

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Nervous systems use excitatory cell assemblies to encode and represent sensory percepts. Similarly, synaptically connected cell assemblies or "engrams" are thought to represent memories of past experience. Multiple lines of recent evidence indicate that brain systems create and use inhibitory replicas of excitatory representations for important cognitive functions. Such matched "inhibitory engrams" can form through homeostatic potentiation of inhibition onto postsynaptic cells that show increased levels of excitation. Inhibitory engrams can reduce behavioral responses to familiar stimuli, thereby resulting in behavioral habituation. In addition, by preventing inappropriate activation of excitatory memory engrams, inhibitory engrams can make memories quiescent, stored in a latent form that is available for contextrelevant activation. In neural networks with balanced excitatory and inhibitory engrams, the release of innate responses and recall of associative memories can occur through focused disinhibition. Understanding mechanisms that regulate the formation and expression of inhibitory engrams in vivo may help not only to explain key features of cognition but also to provide insight into transdiagnostic traits associated with psychiatric conditions such as autism, schizophrenia, and posttraumatic stress disorder.Percepts are thought to be represented in the brain by excitatory activity in groups of neurons, described as cell assemblies (1). Memories may similarly be represented by excitatory connections across different cell assemblies, which form when experiences trigger coordinated activity. Several recent studies indicate that the storage and reactivation of these excitatory "engrams" (2), respectively, may be accompanied by creation and modulation of matched inhibitory engrams. Here, we propose that inhibitory engrams, also termed "negative images" or "inhibitory representations," explain two fundamental features of animal and human psychology: first, behavioral habituation, which allows organisms to ignore familiar, frequently encountered percepts or stimuli, and, second, latent memory, wherein the brain stores tens of thousands of memories in a silent or latent state until recall is required. Such inhibitory engrams can be constructed in neural networks through simple, evolutionarily primitive, synaptic and cellular mechanisms, which are recognized to be involved in the phenomenon of excitatory-inhibitory (EI) balance observed across the brain.Neurons and neural circuits normally operate within a preset range of activity. Outside this range, altered levels of neuronal spiking trigger a variety of homeostatic mechanisms ranging from compensatory ion channel expression to local synaptic scaling (3, 4). These homeostatic mechanisms ensure that the activity parameters of a neuron operate around a set point such that the spiking rates remain stable and a balance of depolarizing and hyperpolarizing currents is maintained. As a consequence, excitation and inhibition are both locally and globally balanced, despite...

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Section: Negative Images In Adaptive Stimulus Filtering and Behavioramentioning

confidence: 71%

Section: Inhibitory Engrams In Associative Memory Storage and Recallmentioning

confidence: 91%

Section: Negative Images In Adaptive Stimulus Filtering and Behavioramentioning

confidence: 99%

Section: Negative Images In Adaptive Stimulus Filtering and Behavioramentioning

confidence: 99%

mentioning

confidence: 99%

See 3 more Smart Citations

Inhibitory engrams in perception and memory

Barron

Vogels

Behrens

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

135

126

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Somatostatin receptors (SSTR1-5) on inhibitory interneurons in the barrel cortex

et al. 2019

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Inhibitory interneurons in the cerebral cortex contain specific proteins or peptides characteristic for a certain interneuron subtype. In mice, three biochemical markers constitute non-overlapping interneuron populations, which account for 80-90% of all inhibitory cells. These interneurons express parvalbumin (PV), somatostatin (SST), or vasoactive intestinal peptide (VIP). SST is not only a marker of a specific interneuron subtype, but also an important neuropeptide that participates in numerous biochemical and signalling pathways in the brain via somatostatin receptors (SSTR1-5). In the nervous system, SST acts as a neuromodulator and neurotransmitter affecting, among others, memory, learning, and mood. In the sensory cortex, the co-localisation of GABA and SST is found in approximately 30% of interneurons. Considering the importance of interactions between inhibitory interneurons in cortical plasticity and the possible GABA and SST co-release, it seems important to investigate the localisation of different SSTRs on cortical interneurons. Here, we examined the distribution of SSTR1-5 on barrel cortex interneurons containing PV, SST, or VIP. Immunofluorescent staining using specific antibodies was performed on brain sections from transgenic mice that expressed red fluorescence in one specific interneuron subtype (PV-Ai14, SST-Ai14, and VIP-Ai14 mice). SSTRs expression on PV, SST, and VIP interneurons varied among the cortical layers and we found two patterns of SSTRs distribution in L4 of barrel cortex. We also demonstrated that, in contrast to other interneurons, PV cells did not express SSTR2, but expressed other SSTRs. SST interneurons, which were not found to make chemical synapses among themselves, expressed all five SSTR subtypes.

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