Different mechanisms are responsible for dishabituation of electrophysiological auditory responses to a change in acoustic identity than to a change in stimulus location

Smulders, Tom V.; Jarvis, Erich D.

doi:10.1016/j.nlm.2013.08.010

Cited by 14 publications

(13 citation statements)

References 46 publications

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“…Our results show the repetition-induced decrease in responses, described by numerous studies both in mammals (Malmierca et al, 2014;Khouri and Nelken, 2015) and songbirds (Chew et al, 1995;Stripling et al, 1997;Phan et al, 2006;Beckers and Gahr, 2012;Smulders and Jarvis, 2013;Lu and Vicario, 2014). Once neuronal responses were decreased, the presentation of a novel song, generally sung by a distinct individual, resets the responses Figure 10.…”

Section: Sensitivity To the Temporal Order Of Syllables In Conspecifisupporting

confidence: 61%

Neuronal Encoding in a High-Level Auditory Area: From Sequential Order of Elements to Grammatical Structure

et al. 2019

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Sensitivity to the sequential structure of communication sounds is fundamental not only for language comprehension in humans but also for song recognition in songbirds. By quantifying single-unit responses, we first assessed whether the sequential order of song elements, called syllables, in conspecific songs is encoded in a secondary auditory cortex-like region of the zebra finch brain. Based on a habituation/ dishabituation paradigm, we show that, after multiple repetitions of the same conspecific song, rearranging syllable order reinstated strong responses. A large proportion of neurons showed sensitivity to song context in which syllables occurred providing support for the nonlinear processing of syllable sequences. Sensitivity to the temporal order of items within a sequence should enable learning its underlying structure, an ability considered a core mechanism of the human language faculty. We show that repetitions of songs that were ordered according to a specific grammatical structure (i.e., ABAB or AABB structures; A and B denoting song syllables) led to different responses in both anesthetized and awake birds. Once responses were decreased due to song repetitions, the transition from one structure to the other could affect the firing rates and/or the spike patterns. Our results suggest that detection was based on local differences rather than encoding of the global song structure as a whole. Our study demonstrates that a high-level auditory region provides neuronal mechanisms to help discriminate stimuli that differ in their sequential structure.Sequence processing has been proposed as a potential precursor of language syntax. As a sequencing operation, the encoding of the temporal order of items within a sequence may help in recognition of relationships between adjacent items and in learning the underlying structure. Taking advantage of the stimulus-specific adaptation phenomenon observed in a high-level auditory region of the zebra finch brain, we addressed this question at the neuronal level. Reordering elements within conspecific songs reinstated robust responses. Neurons also detected changes in the structure of artificial songs, and this detection depended on local transitions between adjacent or nonadjacent syllables. These findings establish the songbird as a model system for deciphering the mechanisms underlying sequence processing at the single-cell level.

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Section: Sensitivity To the Temporal Order Of Syllables In Conspecifisupporting

confidence: 61%

Neuronal Encoding in a High-Level Auditory Area: From Sequential Order of Elements to Grammatical Structure

et al. 2019

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“…Our results in adult animals build on a well-established paradigm in which recent auditory experience is encoded in adult and developing NCM (Chew et al, 1995;Stripling et al, 1997;Smulders and Jarvis, 2013;Miller-Sims and Bottjer, 2014;Ono et al, 2016). As in prior reports, we observed robust auditory recognition memory in the NCM of adults, regardless of treatment group.…”

Section: Recent Auditory Experience Consolidation Is Insensitive To Esupporting

confidence: 86%

Blocking neuroestrogen synthesis modifies neural representations of learned song without altering vocal imitation accuracy in developing songbirds

Hecsh

Remage‐Healey

2019

Preprint

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Birdsong, like human speech, is learned early in life by first memorizing an auditory model. Once memorized, birds compare their own burgeoning vocalizations to their auditory memory, and adjust their song to match the model. While much is known about this latter part of vocal learning, less is known about how initial auditory experiences are formed and consolidated. In both adults and developing songbirds, there is strong evidence suggesting the caudomedial nidopallium (NCM), a higher order auditory forebrain area, is the site of auditory memory consolidation. However, the mechanisms that facilitate this consolidation are poorly understood. One likely mechanism is 17β-estradiol (E2), which is associated with speech-language development and disorders in humans, and is abundant in both mammalian temporal cortex and songbird NCM. Circulating E2 is also elevated during the auditory memory phase, and in NCM immediately after song learning sessions, suggesting it functions to encode recent auditory experience. Therefore, we tested a role for E2 production in auditory memory consolidation during development using a comprehensive set of investigations to ask this question at the level of neuroanatomy, neurophysiology, and behavior. Our results demonstrate that while systemic estrogen synthesis blockade regulates juvenile song production, inhibiting E2 synthesis locally within NCM does not adversely affect song learning outcomes. Surprisingly, early life E2 manipulations in NCM modify the neural representations of birds' own song and the model tutor song in both NCM and a downstream sensorimotor nucleus (HVC). Further, we show that the capacity to synthesize neuroestrogens remains high throughout development alongside substantial changes in NCM cell density across age. Taken together, these findings suggest that E2 plays a multifaceted role during development, and demonstrate that contrary to prediction, unilateral post-training estrogen synthesis blockade in the auditory cortex does not negatively impact vocal learning. Acute downregulation of neuroestrogens are therefore likely permissive for juvenile auditory memorization, while neuroestrogen synthesis influences communication production and representation in adulthood. AntibodiesAntibodies and dilutions for aromatase and parvalbumin were identical to those used in Ikeda et al. (2017). Briefly, we used a polyclonal anti-aromatase primary antibody raised in rabbit (1:2,000; a generous gift from Dr. Colin Saldanha), and a monoclonal anti-parvalbumin primary antibody raised in mouse (1:10,000; Millipore MAB1572; RRID: AB_2174013). Secondary antibodies included goat antirabbit Alexa 488 (1:500; Thermo Fisher Scientific Inc.), and goat anti-mouse Alexa 647 (1:100; Thermo Fisher Scientific Inc.). ProcedureBrain sections were first manually washed 3 x in 0.1 M PB, followed by 3 x 15-minute washes in 0.1 M PB on a plate shaker, followed by a 2-hour incubation at room temperature with 10% normal goat serum (Vector) in 0.3 % PBT. Tissue was then transferred to a 10% normal goat...

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“…Boynton, ; Van Ruijssevelt et al , ). Regarding real‐time in situ neuronal responses, for example, studies using electrophysiology have recorded conspecific‐selective firing patterns from individual neurons at the microsecond scale (Chew et al , ; Chew, Vicario, & Nottebohm, ; Woolley, Hauber, & Theunissen, ; Hauber et al , ; Smulders & Jarvis, ). Brain imaging, such as functional magnetic resonance imaging (fMRI) and positron emission tomography (PET), also showed that conspecific sounds evoke greater neural activity at a stimulus‐length (several seconds) time scale, when compared to sequential playbacks of heterospecific sounds (Poirier et al , ; Louder et al , ; Lattin, Stabile, & Carson, ).…”

Section: Neural Responses To Species‐specific Soundsmentioning

confidence: 99%

“…Several different techniques have demonstrated the role of the avian auditory forebrain in differential processing of acoustic stimuli from different species, even when presenting sounds produced by unfamiliar individuals. Studies using electrophysiology have recorded conspecific‐selective greater firing for neurons within Field L (Woolley et al , ; Hauber et al , ), as well as in the NCM and CMM (Chew et al , , ; Smulders & Jarvis, ). fMRI and PET showed that conspecific sounds evoke greater neural activity when compared to heterospecific sounds (Poirier et al , ; Louder et al , ; Lattin et al , ).…”

Section: Neural Regions Involved In Species‐specific Discriminationmentioning

confidence: 99%

“…The plasticity of neural responses to species‐specific sounds demonstrates that discrimination in the auditory forebrain is not merely a sensory or auditory response, but rather that the neural processing of stimuli is based on the relevance of the auditory signal to the receiver. In the short‐term, neurons habituate to repeated exposure to the same stimuli as each repeated presentation provides less information, such that repeated presentations of heterospecific songs cause neurons within the auditory forebrain to habituate much more rapidly compared to repeated exposure to conspecific songs (Smulders & Jarvis, ). Heterospecific‐induced cellular habituation also lasts for a shorter duration (Chew et al , , ).…”

Section: Recognition Of Species‐specific Soundsmentioning

confidence: 99%

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Neural mechanisms of auditory species recognition in birds

et al. 2019

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Auditory communication in humans and other animals frequently takes place in noisy environments with many co‐occurring signallers. Receivers are thus challenged to rapidly recognize salient auditory signals and filter out irrelevant sounds. Most bird species produce a variety of complex vocalizations that function to communicate with other members of their own species and behavioural evidence broadly supports preferences for conspecific over heterospecific sounds (auditory species recognition). However, it remains unclear whether such auditory signals are categorically recognized by the sensory and central nervous system. Here, we review 53 published studies that compare avian neural responses between conspecific versus heterospecific vocalizations. Irrespective of the techniques used to characterize neural activity, distinct nuclei of the auditory forebrain are consistently shown to be repeatedly conspecific selective across taxa, even in response to unfamiliar individuals with distinct acoustic properties. Yet, species‐specific neural discrimination is not a stereotyped auditory response, but is modulated according to its salience depending, for example, on ontogenetic exposure to conspecific versus heterospecific stimuli. Neuromodulators, in particular norepinephrine, may mediate species recognition by regulating the accuracy of neuronal coding for salient conspecific stimuli. Our review lends strong support for neural structures that categorically recognize conspecific signals despite the highly variable physical properties of the stimulus. The available data are in support of a ‘perceptual filter’‐based mechanism to determine the saliency of the signal, in that species identity and social experience combine to influence the neural processing of species‐specific auditory stimuli. Finally, we present hypotheses and their testable predictions, to propose next steps in species‐recognition research into the emerging model of the neural conceptual construct in avian auditory recognition.

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Different mechanisms are responsible for dishabituation of electrophysiological auditory responses to a change in acoustic identity than to a change in stimulus location

Cited by 14 publications

References 46 publications

Neuronal Encoding in a High-Level Auditory Area: From Sequential Order of Elements to Grammatical Structure

Neuronal Encoding in a High-Level Auditory Area: From Sequential Order of Elements to Grammatical Structure

Blocking neuroestrogen synthesis modifies neural representations of learned song without altering vocal imitation accuracy in developing songbirds

Neural mechanisms of auditory species recognition in birds

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