Neuronal populations and single cells representing learned auditory objects

Gentner, Timothy Q.; Margoliash, Daniel

doi:10.1038/nature01731

Cited by 234 publications

(208 citation statements)

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“…Learned visual associations in monkeys are reflected by association-selective representations in higher visual areas of the temporal cortex (21,22), with top-down activation by the PFC contributing to prospective representations of the choice picture to be recalled (19). Changes to stimulus-selective representations in higher sensory areas have also been reported in anesthetized starlings trained on auditory discriminations (23)(24)(25). Single neurons as well as population activity in auditory association areas contained information about the behavioral relevance of different sounds.…”

Section: Discussionmentioning

confidence: 90%

Associative learning rapidly establishes neuronal representations of upcoming behavioral choices in crows

Veit

Pidpruzhnykova

Nieder

2015

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

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The ability to form associations between behaviorally relevant sensory stimuli is fundamental for goal-directed behaviors. We investigated neuronal activity in the telencephalic area nidopallium caudolaterale (NCL) while two crows (Corvus corone) performed a delayed association task. Whereas some paired associates were familiar to the crows, novel associations had to be learned and mapped to the same target stimuli within a single session. We found neurons that prospectively encoded the chosen test item during the delay for both familiar and newly learned associations. These neurons increased their selectivity during learning in parallel with the crows' increased behavioral performance. Thus, sustained activity in the NCL actively processes information for the upcoming behavioral choice. These data provide new insights into memory representations of behaviorally meaningful stimuli in birds, and how such representations are formed during learning. The findings suggest that the NCL plays a role in learning arbitrary associations, a cornerstone of corvids' remarkable behavioral flexibility and adaptability.association learning | crow | single-cell recordings | nidopallium caudolaterale | memory T he ability to form arbitrary associations between sensory stimuli is fundamental for many flexible goal-directed behaviors. Corvids exploit learned associations intensively when adapting their behavior to a changing environment (1, 2). For example, scrub jays learn to associate different foods with different degradation speeds as a component of their episodic-like memory during food-caching behavior (3). The neuronal basis of corvids' ability to learn arbitrary associations has never been investigated.The avian cognitive integration area nidopallium caudolaterale (NCL) is a good candidate to investigate learning-related changes in the representation of initially unknown stimuli, as they acquire behavioral meaning during association learning. We have recently demonstrated that single NCL neurons encode abstract behavioral rules, irrespective of the arbitrary, learned cues used to instruct the rule (4). Furthermore, pigeons with lesions of the NCL show deficits in a reversal learning task, indicating that the NCL is a crucial structure to flexibly adapt behavior based on feedback during learning (5). The NCL is the main pallial target of dopaminergic projections from the midbrain (6), and dopamine signaling in striatal and cortical structures is involved in learning and memory processes in birds, as in mammals (7).Here we investigate changes in the neuronal representation while associative learning links arbitrary visual items in memory. We trained two carrion crows on a delayed paired-association learning (DPA) task and recorded NCL neurons during the course of learning. The task design allowed us to compare neuronal responses during the mapping of highly familiar images onto test items, as well as to follow the emergence of associative signals in the same neurons while the crows learned to map novel sample images onto the ...

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Section: Discussionmentioning

confidence: 90%

Associative learning rapidly establishes neuronal representations of upcoming behavioral choices in crows

Veit

Pidpruzhnykova

Nieder

2015

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

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“…Measurement of long-term response habituation in NCM, by both electrophysiology and the study of the song stimulation-induced up-regulation of ZENK, has suggested that this area might encode the long-lasting sensory memory of the TUT (31,40). Other experiments point to the fact that NCM and CM might be involved in short-term plasticity related to song discrimination (18,19,48). The greater representation of TUT and BOS revealed by fMRI in our experiments therefore might reflect an important aspect of the sensory memory for these developmentally salient familiar stimuli.…”

Section: Familiar Song Stimuli Show Selective Differential Topographymentioning

confidence: 99%

“…In parallel with song motor learning, auditory song selectivity gradually emerges during development (13)(14)(15)(16)(17). Robust sensory responses to auditory stimuli have been recorded in the primary auditory area in the caudal telencephalic region (field L), the caudomedial nidopallium (NCM), the caudal mesopallium (CM), and the caudomedial ventral hyperstriatum (18)(19)(20)(21), as well as in the song nuclei HVC, LMAN, X, and nucleus interface of the nidopallium (22)(23)(24)(25)(26)(27)(28). Sensory representation of birdsong in the song nuclei and the secondary auditory areas NCM and CM is characterized by response selectivity to song ownership, familiarity, and species-specific features.…”

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confidence: 99%

Functional MRI of the zebra finch brain during song stimulation suggests a lateralized response topography

Voss

Tabelow

Polzehl

et al. 2007

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

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Electrophysiological and activity-dependent gene expression studies of birdsong have contributed to the understanding of the neural representation of natural sounds. However, we have limited knowledge about the overall spatial topography of song representation in the avian brain. Here, we adapt the noninvasive functional MRI method in mildly sedated zebra finches (Taeniopygia guttata) to localize and characterize song driven brain activation. Based on the blood oxygenation level-dependent signal, we observed a differential topographic responsiveness to playback of bird's own song, tutor song, conspecific song, and a pure tone as a nonsong stimulus. The bird's own song caused a stronger response than the tutor song or tone in higher auditory areas. This effect was more pronounced in the medial parts of the forebrain. We found left-right hemispheric asymmetry in sensory responses to songs, with significant discrimination between stimuli observed only in the right hemisphere. This finding suggests that perceptual responses might be lateralized in zebra finches. In addition to establishing the feasibility of functional MRI in sedated songbirds, our results demonstrate spatial coding of song in the zebra finch forebrain, based on developmental familiarity and experience.imaging ͉ learning ͉ memory B irdsong is studied as a model of vocal learning, perception, production, and motor abnormalities of speech (1, 2). There are interesting parallels between song development and speech development (3) and between auditory and vocal pathways in the songbird and human brain (4). Therefore, insights from experiments on songbirds may contribute to the understanding of auditory and vocal function in humans. For example, minimal models of speech dyspraxia (5) and dysfluencies such as stuttering are being developed in zebra finches (6). Zebra finches are capable of learning, producing, perceiving, and discriminating complex sound patterns. Birdsong in zebra finches consists of a sequence of distinctive sounds produced by males and is characterized by a consistent and reproducible acoustic profile. Song is learned by imitating the song of an adult conspecific tutor during a sensitive period of development (7-10). Recently, it has been shown that songbirds are able to learn recursive syntactic patterns, presumably a simple form of grammar (11), thus extending the potential applicability of the birdsong model to our understanding of the biological basis of languages. Several brain structures are required for learning, production, and perception of birdsong. It is known from electrophysiological studies that song learning nuclei, such as the lateral magnocellular nucleus of the anterior nidopallium (LMAN) and X (12), play an important role in song development. In parallel with song motor learning, auditory song selectivity gradually emerges during development (13-17). Robust sensory responses to auditory stimuli have been recorded in the primary auditory area in the caudal telencephalic region (field L), the caudomedial nidopallium (N...

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“…Nevertheless, female zebra finches can learn to recognize songs to which they have been exposed, and they develop a preference for these songs (Riebel, 2000;Riebel et al, 2002). Several studies have shown that both the NCM and the CMHV are involved in processing conspecific songs in female songbirds (Chew et al, 1996;MacDougall-Shackleton et al, 1998;Duffy et al, 1999;Gentner et al, 2001;Bailey et al, 2002;Sockman et al, 2002;Bailey and Wade, 2003;Gentner and Margoliash, 2003;Grace et al, 2003;Maney et al, 2003;Phillmore et al, 2003), as well as in female budgerigars . Preliminary results from our own laboratory indicate that, in female zebra finches, the CMHV may be part of the neural representation of learned tutor song (Terpstra et al, 2001).…”

Section: The Role Of the Cmhv In Tutor Song Representationmentioning

confidence: 99%

An Analysis of the Neural Representation of Birdsong Memory

Terpstra¹,

Bolhuis²,

Boer-Visser³

2004

J. Neurosci.

125

141

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Songbirds, such as zebra finches, learn their song from a tutor early in life. Forebrain nuclei in the "song system" are important for the acquisition and production of song. Brain regions [including the caudomedial part of the neostriatum (NCM) and of the hyperstriatum ventrale (CMHV)] outside the song system show increased neuronal activation, measured as expression of immediate early genes (IEGs), when zebra finch males are exposed to song. IEG expression in the NCM in response to tutor song is significantly positively correlated with the strength of song learning (i.e., the number of elements copied). Here, we exposed three groups of adult zebra finch males to tutor song, to their own song, or to novel conspecific song. The two control groups were included to examine an alternative explanation of our previous results in terms of variation in predisposed levels of attentiveness. Expression of Zenk, the protein product of the IEG ZENK, was measured in the NCM, CMHV, and hippocampus. There were no significant differences in overall Zenk expression between the three experimental groups. However, there was a significant positive correlation between Zenk expression in the NCM (but not in the other two regions) and strength of song learning in the males that were exposed to the tutor song. There was no such correlation in the other two groups. These results suggest that experience-related neuronal activation is specific to the tutor song and thus unlikely to be a result of differences in attention.

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Neuronal populations and single cells representing learned auditory objects

Cited by 234 publications

References 24 publications

Associative learning rapidly establishes neuronal representations of upcoming behavioral choices in crows

Associative learning rapidly establishes neuronal representations of upcoming behavioral choices in crows

Functional MRI of the zebra finch brain during song stimulation suggests a lateralized response topography

An Analysis of the Neural Representation of Birdsong Memory

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