Inhibition protects acquired song segments during vocal learning in zebra finches

Vallentin, Daniela; Kosche, Georg; Lipkind, Dina; Long, Michael A.

doi:10.1126/science.aad3023

Cited by 125 publications

(119 citation statements)

References 38 publications

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“…These findings are consistent with electrophysiological recordings in a songbird while it listens to a tutor's song (41) (Fig. 4 F-H).…”

Section: Inhibitory Engrams In Associative Memory Storage and Recallsupporting

confidence: 88%

“…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: 92%

“…Similarly, memory is first encoded as excitatory engrams. Over time, matched inhibitory engrams form to rebalance the neural network (11,41). The formation of these inhibitory memory engrams may occur via homeostatic mechanisms similar to those mechanisms involved in habituation, potentially during replay of excitatory memory engrams.…”

Section: A Framework For Normal and Variant Memory Storage And Recallmentioning

confidence: 99%

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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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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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“…These findings are consistent with electrophysiological recordings in a songbird while it listens to a tutor's song (41) (Fig. 4 F-H).…”

Section: Inhibitory Engrams In Associative Memory Storage and Recallsupporting

confidence: 88%

Section: Inhibitory Engrams In Associative Memory Storage and Recallmentioning

confidence: 92%

Section: A Framework For Normal and Variant Memory Storage And Recallmentioning

confidence: 99%

See 1 more Smart Citation

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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“…To quantify this effect on response time, we calculated a precision measure [49] that estimates deviation from a uniform distribution of response latencies as a z-score. After lesioning, precision of responses to ICs decreases from 4.43 ±0.37 to 1.91±0.25 (paired t-test, n=5 birds, p<0.01, Figure 4C, top).…”

Section: Resultsmentioning

confidence: 99%

The Forebrain Song System Mediates Predictive Call Timing in Female and Male Zebra Finches

et al. 2016

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SUMMARY The dichotomy between vocal learners and non-learners is a fundamental distinction in the study of animal communication. Male zebra finches (Taeniopygia guttata) are vocal learners that acquire a song resembling their tutors’, whereas females can only produce innate calls. The acoustic structure of short calls, produced by both males and females, is not learned. However, these calls can be precisely coordinated across individuals. To examine how birds learn to synchronize their calls, we developed a vocal robot that exchanges calls with a partner bird. Because birds answer the robot with stereotyped latencies, we could program it to disrupt each bird’s responses by producing calls that are likely to coincide with the bird’s. Within minutes, the birds learned to avoid this disruptive masking (jamming) by adjusting the timing of their responses. Notably, females exhibited greater adaptive timing plasticity than males. Further, when challenged with complex rhythms containing jamming elements, birds dynamically adjusted the timing of their calls in anticipation of jamming. Blocking the song system cortical output dramatically reduced the precision of birds’ response timing and abolished their ability to avoid jamming. Surprisingly, we observed this effect in both males and females, indicating that the female song system is functional rather than vestigial. We suggest that descending forebrain projections, including the song-production pathway, function as a general-purpose sensorimotor communication system. In the case of calls, it enables plasticity in vocal timing to facilitate social interactions, whereas in the case of songs, plasticity extends to developmental changes in vocal structure.

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“…HVC interneurons play a significant role in several models of sequence generation and learning in HVC (Amador et al, 2013;Dutar et al, 1998;Kosche et al, 2015;Long et al, 2010;Markowitz et al, 2015;Marler and Peters, 1982;Mooney and Prather, 2005;Vallentin et al, 2016), and some models make specific predictions about the relative timing of interneuron and PN activity. For example, the GTE model predicts that local minima in the firing rate modulations of HVC interneurons coincide with GTEs (Amador et al, 2013).…”

Section: Coordination Of Hvc Pn and Interneuron Activitymentioning

confidence: 99%

Rhythmic Continuous-Time Coding in the Songbird Analog of Vocal Motor Cortex

Lynch

Okubo

Hanuschkin

et al. 2016

Neuron

154

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Songbirds learn and produce complex sequences of vocal gestures. Adult birdsong requires premotor nucleus HVC, in which projection neurons (PNs) burst sparsely at stereotyped times in the song. It has been hypothesized that PN bursts, as a population, form a continuous sequence, while a different model of HVC function proposes that both HVC PN and interneuron activity is tightly organized around motor gestures. Using a large dataset of PNs and interneurons recorded in singing birds, we test several predictions of these models. We find that PN bursts in adult birds are continuously and nearly uniformly distributed throughout song. However, we also find that PN and interneuron firing rates exhibit significant 10-Hz rhythmicity locked to song syllables, peaking prior to syllable onsets and suppressed prior to offsets-a pattern that predominates PN and interneuron activity in HVC during early stages of vocal learning.

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Inhibition protects acquired song segments during vocal learning in zebra finches

Cited by 125 publications

References 38 publications

Inhibitory engrams in perception and memory

Inhibitory engrams in perception and memory

The Forebrain Song System Mediates Predictive Call Timing in Female and Male Zebra Finches

Rhythmic Continuous-Time Coding in the Songbird Analog of Vocal Motor Cortex

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