Pauses during communication release behavioral habituation through recovery from synaptic depression

Kohashi, Tsunehiko; Lube, Adalee; Yang, Jenny; Roberts-Gaddipati, Prema S.; Carlson, Bruce A.

doi:10.1016/j.cub.2021.04.056

Cited by 5 publications

(5 citation statements)

References 40 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Also, recovery from STSD during communication pauses has been linked to maximising the effect of post-pause communication signals (Kohashi et al. 2021 ). Computational models show that STSD accounts for different forms of context sensitivity in the AC (Loebel et al.…”

Section: Introductionmentioning

confidence: 99%

Auditory cortex modelled as a dynamical network of oscillators: understanding event-related fields and their adaptation

et al. 2022

View full text Add to dashboard Cite

Adaptation, the reduction of neuronal responses by repetitive stimulation, is a ubiquitous feature of auditory cortex (AC). It is not clear what causes adaptation, but short-term synaptic depression (STSD) is a potential candidate for the underlying mechanism. In such a case, adaptation can be directly linked with the way AC produces context-sensitive responses such as mismatch negativity and stimulus-specific adaptation observed on the single-unit level. We examined this hypothesis via a computational model based on AC anatomy, which includes serially connected core, belt, and parabelt areas. The model replicates the event-related field (ERF) of the magnetoencephalogram as well as ERF adaptation. The model dynamics are described by excitatory and inhibitory state variables of cell populations, with the excitatory connections modulated by STSD. We analysed the system dynamics by linearising the firing rates and solving the STSD equation using time-scale separation. This allows for characterisation of AC dynamics as a superposition of damped harmonic oscillators, so-called normal modes. We show that repetition suppression of the N1m is due to a mixture of causes, with stimulus repetition modifying both the amplitudes and the frequencies of the normal modes. In this view, adaptation results from a complete reorganisation of AC dynamics rather than a reduction of activity in discrete sources. Further, both the network structure and the balance between excitation and inhibition contribute significantly to the rate with which AC recovers from adaptation. This lifetime of adaptation is longer in the belt and parabelt than in the core area, despite the time constants of STSD being spatially homogeneous. Finally, we critically evaluate the use of a single exponential function to describe recovery from adaptation.

show abstract

Section: Introductionmentioning

confidence: 99%

Auditory cortex modelled as a dynamical network of oscillators: understanding event-related fields and their adaptation

et al. 2022

View full text Add to dashboard Cite

show abstract

“…Carlson and Hopkins ( 2004b ) demonstrated the existence of three different modal classes of SPI displays (accelerations, scallops, and rasps) with an increased firing rate that differs categorically in their temporal structure. As scallops are defined by a pause in the EOD generation, they also define a fourth categorically different display (Moller, 1970 ; Moller et al, 1989 ; Kohashi et al, 2021 ).…”

Section: Computational Model Of the Electromotor Command Networkmentioning

confidence: 99%

“…Finally, cessations (refer to Figure 2 ) correspond to activity dropping in the EOD generation for periods up to 1 s. A cessation is evoked by the activation of the ventroposterior nucleus (VPd, refer to Figure 1 ). Submissive behavior has been associated with this SPI (Moller, 1970 ; Moller et al, 1989 ), and it has also been related to increased sensitivity to receiving communication signals (Kohashi et al, 2021 ). We will use these four representative patterns to validate our electromotor network modeling approach.…”

Section: Computational Model Of the Electromotor Command Networkmentioning

confidence: 99%

Modeling the Sequential Pattern Variability of the Electromotor Command System of Pulse Electric Fish

Lareo

Varona

Rodríguez

2022

Front. Neuroinform.

View full text Add to dashboard Cite

Mormyridae, a family of weakly electric fish, use electric pulses for communication and for extracting information from the environment (active electroreception). The electromotor system controls the timing of pulse generation. Ethological studies have described several sequences of pulse intervals (SPIs) related to distinct behaviors (e.g., mating or exploratory behaviors). Accelerations, scallops, rasps, and cessations are four different SPI patterns reported in these fish, each showing characteristic stereotyped temporal structures. This article presents a computational model of the electromotor command circuit that reproduces a whole set of SPI patterns while keeping the same internal network configuration. The topology of the model is based on a simplified representation of the network with four neuron clusters (nuclei). An initial configuration was built to reproduce nucleus characteristics and network topology as described by detailed morphological and electrophysiological studies. Then, a methodology based on a genetic algorithm (GA) was developed and applied to tune the model connectivity parameters to automatically reproduce a whole set of patterns recorded from freely-behaving Gnathonemus petersii specimens. Robustness analyses of input variability were performed to discard overfitting and assess validity. Results show that the set of SPI patterns is consistently reproduced reaching a dynamic balance between synaptic properties in the network. This model can be used as a tool to test novel hypotheses regarding temporal structure in electrogeneration. Beyond the electromotor model itself, the proposed methodology can be adapted to fit models of other biological networks that also exhibit sequential patterns.

show abstract

“…For example, similar to humans, epochs of silence in acoustic signaling provide information that allow interacting individuals to minimize overlap in the timing of their vocalizations (Benichov et al., 2016; Brumm, 2006; Egnor et al., 2007; Hultsch & Todt, 1982; Zelick & Narins, 1983). On a finer temporal scale, the duration of silent gaps between distinct components of signals provides information about individual and species identity in various species, including crickets, frogs, and birds (Araki et al., 2016; Coen et al., 2014; Feng et al., 1990; Gerhardt, 2005; Hedwig, 2006; Ronacher et al., 2015) and can help receivers infer arousal levels and other aspects of signaler condition (Cooper & Goller, 2006; James & Sakata, 2014; James & Sakata, 2015, 2019; Chen et al., 2016; Kohashi et al., 2021). Despite the similarities in the information content provided by the temporal organization of communicative elements across humans and non‐human animals, relatively little is known about how biological predispositions and developmental experiences shape the temporal organization of communication signals.…”

Section: Introductionmentioning

confidence: 99%

Learning to pause: Fidelity of and biases in the developmental acquisition of gaps in the communicative signals of a songbird

James

Wang

Bertolo

et al. 2023

Developmental Science

View full text Add to dashboard Cite

The temporal organization of sounds used in social contexts can provide information about signal function and evoke varying responses in listeners (receivers). For example, music is a universal and learned human behavior that is characterized by different rhythms and tempos that can evoke disparate responses in listeners. Similarly, birdsong is a social behavior in songbirds that is learned during critical periods in development and used to evoke physiological and behavioral responses in receivers. Recent investigations have begun to reveal the breadth of universal patterns in birdsong and their similarities to common patterns in speech and music, but relatively little is known about the degree to which biological predispositions and developmental experiences interact to shape the temporal patterning of birdsong. Here, we investigated how biological predispositions modulate the acquisition and production of an important temporal feature of birdsong, namely the duration of silent pauses (“gaps”) between vocal elements (“syllables”). Through analyses of semi‐naturally raised and experimentally tutored zebra finches, we observed that juvenile zebra finches imitate the durations of the silent gaps in their tutor's song. Further, when juveniles were experimentally tutored with stimuli containing a wide range of gap durations, we observed biases in the prevalence and stereotypy of gap durations. Together, these studies demonstrate how biological predispositions and developmental experiences differently affect distinct temporal features of birdsong and highlight similarities in developmental plasticity across birdsong, speech, and music.Research Highlights The temporal organization of learned acoustic patterns can be similar across human cultures and across species, suggesting biological predispositions in acquisition. We studied how biological predispositions and developmental experiences affect an important temporal feature of birdsong, namely the duration of silent intervals between vocal elements (“gaps”). Semi‐naturally and experimentally tutored zebra finches imitated the durations of gaps in their tutor's song and displayed some biases in the learning and production of gap durations and in gap variability. These findings in the zebra finch provide parallels with the acquisition of temporal features of speech and music in humans.

show abstract

Pauses during communication release behavioral habituation through recovery from synaptic depression

Cited by 5 publications

References 40 publications

Auditory cortex modelled as a dynamical network of oscillators: understanding event-related fields and their adaptation

Auditory cortex modelled as a dynamical network of oscillators: understanding event-related fields and their adaptation

Modeling the Sequential Pattern Variability of the Electromotor Command System of Pulse Electric Fish

Learning to pause: Fidelity of and biases in the developmental acquisition of gaps in the communicative signals of a songbird

Contact Info

Product

Resources

About