Is the MSB hypothesis (music as a coevolved system for social bonding) testable in the Popperian sense?

"Music As a Coevolved System for Social Bonding" (MSB) is a brilliant synthesis and appealing hypothesis offering insights into the evolution and social bonding of musicality, but is so broad and sweeping it will be challenging to test, prove or falsify in the Popperian sense (Popper, 1959). After general comments, I focus my critique on underlying neurobiological mechanisms, and offer some suggestions for experimental tests of MSB.

Dorsal prefrontal and premotor cortex of the ferret as defined by distinctive patterns of thalamo-cortical projections.

Recent studies of the neurobiology of the dorsal frontal cortex (FC) of the ferret have illuminated its key role in the attention network, top-down cognitive control of sensory processing, and goal directed behavior. To elucidate the neuroanatomical regions of the dorsal FC, and delineate the boundary between premotor cortex (PMC) and dorsal prefrontal cortex (dPFC), we placed retrograde tracers in adult ferret dorsal FC anterior to primary motor cortex and analyzed thalamo-cortical connectivity. Cyto- and myeloarchitectural differences across dorsal FC and the distinctive projection patterns from thalamic nuclei, especially from the subnuclei of the medial dorsal (MD) nucleus and the ventral thalamic nuclear group, make it possible to clearly differentiate three separate dorsal FC fields anterior to primary motor cortex: polar dPFC (dPFCpol), dPFC, and PMC. Based on the thalamic connectivity, there is a striking similarity of the ferret's dorsal FC fields with other species. This possible homology opens up new questions for future comparative neuroanatomical and functional studies.

Dynamics and Hierarchical Encoding of Non-compact Acoustic Categories in Auditory and Frontal Cortex.

Categorical perception is a fundamental cognitive function enabling animals to flexibly assign sounds into behaviorally relevant categories. This study investigates the nature of acoustic category representations, their emergence in an ascending series of ferret auditory and frontal cortical fields, and the dynamics of this representation during passive listening to task-relevant stimuli and during active retrieval from memory while engaging in learned categorization tasks. Ferrets were trained on two auditory Go-NoGo categorization tasks to discriminate two non-compact sound categories (composed of tones or amplitude-modulated noise). Neuronal responses became progressively more categorical in higher cortical fields, especially during task performance. The dynamics of the categorical responses exhibited a cascading top-down modulation pattern that began earliest in the frontal cortex and subsequently flowed downstream to the secondary auditory cortex, followed by the primary auditory cortex. In a subpopulation of neurons, categorical responses persisted even during the passive listening condition, demonstrating memory for task categories and their enhanced categorical boundaries.

What can animal communication teach us about human language?

Language has been considered by many to be uniquely human. Numerous theories for how it evolved have been proposed but rarely tested. The articles in this theme issue consider the extent to which aspects of language, such as vocal learning, phonology, syntax, semantics, intentionality, cognition and neurobiological adaptations, are shared with other animals. By adopting a comparative approach, insights into the mechanisms and origins of human language can be gained. While points of agreement exist among the authors, conflicting viewpoints are expressed on several issues, such as the presence of proto-syntax in animal communication, the neural basis of the Merge operation, and the neurogenetic changes necessary for vocal learning. Future comparative research in animal communication has the potential to teach us even more about the evolution, neurobiology and cognitive basis of human language. This article is part of the theme issue 'What can animal communication teach us about human language?'

Adaptive Efficient Coding of Correlated Acoustic Properties.

Natural sounds such as vocalizations often have covarying acoustic attributes, resulting in redundancy in neural coding. The efficient coding hypothesis proposes that sensory systems are able to detect such covariation and adapt to reduce redundancy, leading to more efficient neural coding. Recent psychoacoustic studies have shown the auditory system can rapidly adapt to efficiently encode two covarying dimensions as a single dimension, following passive exposure to sounds in which temporal and spectral attributes covaried in a correlated fashion. However, these studies observed a cost to this adaptation, which was a loss of sensitivity to the orthogonal dimension. Here we explore the neural basis of this psychophysical phenomenon by recording single-unit responses from the primary auditory cortex in awake ferrets exposed passively to stimuli with two correlated attributes, similar in stimulus design to the psychoacoustic experiments in humans. We found: (1) the signal-to-noise ratio of spike-rate coding of cortical responses driven by sounds with correlated attributes remained unchanged along the exposure dimension, but was reduced along the orthogonal dimension; (2) performance of a decoder trained with spike data to discriminate stimuli along the orthogonal dimension was equally reduced; (3) correlations between neurons tuned to the two covarying attributes decreased after exposure; and (4) these exposure effects still occurred if sounds were correlated along two acoustic dimensions, but varied randomly along a third dimension. These neurophysiological results are consistent with the efficient coding hypothesis and may help deepen our understanding of how the auditory system encodes and represents acoustic regularities and covariance.SIGNIFICANCE STATEMENT The efficient coding (EC) hypothesis (Attneave, 1954; Barlow, 1961) proposes that the neural code in sensory systems efficiently encodes natural stimuli by minimizing the number of spikes to transmit a sensory signal. Results of recent psychoacoustic studies in humans are consistent with the EC hypothesis in that, following passive exposure to stimuli with correlated attributes, the auditory system rapidly adapts so as to more efficiently encode the two covarying dimensions as a single dimension. In the current neurophysiological experiments, using a similar stimulus design and the experimental paradigm to the psychoacoustic studies of Stilp et al. (2010) and Stilp and Kluender (2011, 2012, 2016), we recorded responses from single neurons in the auditory cortex of the awake ferret, showing adaptive efficient neural coding of two correlated acoustic attributes.

Computational Neural Modeling of Auditory Cortical Receptive Fields.

Previous studies have shown that the auditory cortex can enhance the perception of behaviorally important sounds in the presence of background noise, but the mechanisms by which it does this are not yet elucidated. Rapid plasticity of spectrotemporal receptive fields (STRFs) in the primary (A1) cortical neurons is observed during behavioral tasks that require discrimination of particular sounds. This rapid task-related change is believed to be one of the processing strategies utilized by the auditory cortex to selectively attend to one stream of sound in the presence of mixed sounds. However, the mechanism by which the brain evokes this rapid plasticity in the auditory cortex remains unclear. This paper uses a neural network model to investigate how synaptic transmission within the cortical neuron network can change the receptive fields of individual neurons. A sound signal was used as input to a model of the cochlea and auditory periphery, which activated or inhibited integrate-and-fire neuron models to represent networks in the primary auditory cortex. Each neuron in the network was tuned to a different frequency. All neurons were interconnected with excitatory or inhibitory synapses of varying strengths. Action potentials in one of the model neurons were used to calculate the receptive field using reverse correlation. The results were directly compared to previously recorded electrophysiological data from ferrets performing behavioral tasks that require discrimination of particular sounds. The neural network model could reproduce complex STRFs observed experimentally through optimizing the synaptic weights in the model. The model predicts that altering synaptic drive between cortical neurons and/or bottom-up synaptic drive from the cochlear model to the cortical neurons can account for rapid task-related changes observed experimentally in A1 neurons. By identifying changes in the synaptic drive during behavioral tasks, the model provides insights into the neural mechanisms utilized by the auditory cortex to enhance the perception of behaviorally salient sounds.

State-dependent encoding of sound and behavioral meaning in a tertiary region of the ferret auditory cortex.

In higher sensory cortices, there is a gradual transformation from sensation to perception and action. In the auditory system, this transformation is revealed by responses in the rostral ventral posterior auditory field (VPr), a tertiary area in the ferret auditory cortex, which shows long-term learning in trained compared to naïve animals, arising from selectively enhanced responses to behaviorally relevant target stimuli. This enhanced representation is further amplified during active performance of spectral or temporal auditory discrimination tasks. VPr also shows sustained short-term memory activity after target stimulus offset, correlated with task response timing and action. These task-related changes in auditory filter properties enable VPr neurons to quickly and nimbly switch between different responses to the same acoustic stimuli, reflecting either spectrotemporal properties, timing, or behavioral meaning of the sound. Furthermore, they demonstrate an interaction between the dynamics of short-term attention and long-term learning, as incoming sound is selectively attended, recognized, and translated into action.

Laminar profile of task-related plasticity in ferret primary auditory cortex.

Rapid task-related plasticity is a neural correlate of selective attention in primary auditory cortex (A1). Top-down feedback from higher-order cortex may drive task-related plasticity in A1, characterized by enhanced neural representation of behaviorally meaningful sounds during auditory task performance. Since intracortical connectivity is greater within A1 layers 2/3 (L2/3) than in layers 4-6 (L4-6), we hypothesized that enhanced representation of behaviorally meaningful sounds might be greater in A1 L2/3 than L4-6. To test this hypothesis and study the laminar profile of task-related plasticity, we trained 2 ferrets to detect pure tones while we recorded laminar activity across a 1.8 mm depth in A1. In each experiment we analyzed high-gamma local field potentials (LFPs) and multi-unit spiking in response to identical acoustic stimuli during both passive listening and active task performance. We found that neural responses to auditory targets were enhanced during task performance, and target enhancement was greater in L2/3 than in L4-6. Spectrotemporal receptive fields (STRFs) computed from both high-gamma LFPs and multi-unit spiking showed similar increases in auditory target selectivity, also greatest in L2/3. Our results suggest that activity within intracortical networks plays a key role in the underlying neural mechanisms of selective attention.

Implicit Memory for Complex Sounds in Higher Auditory Cortex of the Ferret.

Responses of auditory cortical neurons encode sound features of incoming acoustic stimuli and also are shaped by stimulus context and history. Previous studies of mammalian auditory cortex have reported a variable time course for such contextual effects ranging from milliseconds to minutes. However, in secondary auditory forebrain areas of songbirds, long-term stimulus-specific neuronal habituation to acoustic stimuli can persist for much longer periods of time, ranging from hours to days. Such long-term habituation in the songbird is a form of long-term auditory memory that requires gene expression. Although such long-term habituation has been demonstrated in avian auditory forebrain, this phenomenon has not previously been described in the mammalian auditory system. Utilizing a similar version of the avian habituation paradigm, we explored whether such long-term effects of stimulus history also occur in auditory cortex of a mammalian auditory generalist, the ferret. Following repetitive presentation of novel complex sounds, we observed significant response habituation in secondary auditory cortex, but not in primary auditory cortex. This long-term habituation appeared to be independent for each novel stimulus and often lasted for at least 20 min. These effects could not be explained by simple neuronal fatigue in the auditory pathway, because time-reversed sounds induced undiminished responses similar to those elicited by completely novel sounds. A parallel set of pupillometric response measurements in the ferret revealed long-term habituation effects similar to observed long-term neural habituation, supporting the hypothesis that habituation to passively presented stimuli is correlated with implicit learning and long-term recognition of familiar sounds.SIGNIFICANCE STATEMENT Long-term habituation in higher areas of songbird auditory forebrain is associated with gene expression and is correlated with recognition memory. Similar long-term auditory habituation in mammals has not been previously described. We studied such habituation in single neurons in the auditory cortex of awake ferrets that were passively listening to repeated presentations of various complex sounds. Responses exhibited long-lasting habituation (at least 20 min) in the secondary, but not primary auditory cortex. Habituation ceased when stimuli were played backward, despite having identical spectral content to the original sound. This long-term neural habituation correlated with similar habituation of ferret pupillary responses to repeated presentations of the same stimuli, suggesting that stimulus habituation is retained as a long-term behavioral memory.

Extracting neuronal functional network dynamics via adaptive Granger causality analysis.

Quantifying the functional relations between the nodes in a network based on local observations is a key challenge in studying complex systems. Most existing time series analysis techniques for this purpose provide static estimates of the network properties, pertain to stationary Gaussian data, or do not take into account the ubiquitous sparsity in the underlying functional networks. When applied to spike recordings from neuronal ensembles undergoing rapid task-dependent dynamics, they thus hinder a precise statistical characterization of the dynamic neuronal functional networks underlying adaptive behavior. We develop a dynamic estimation and inference paradigm for extracting functional neuronal network dynamics in the sense of Granger, by integrating techniques from adaptive filtering, compressed sensing, point process theory, and high-dimensional statistics. We demonstrate the utility of our proposed paradigm through theoretical analysis, algorithm development, and application to synthetic and real data. Application of our techniques to two-photon Ca2+ imaging experiments from the mouse auditory cortex reveals unique features of the functional neuronal network structures underlying spontaneous activity at unprecedented spatiotemporal resolution. Our analysis of simultaneous recordings from the ferret auditory and prefrontal cortical areas suggests evidence for the role of rapid top-down and bottom-up functional dynamics across these areas involved in robust attentive behavior.

Orbitofrontal Cortex Neurons Respond to Sound and Activate Primary Auditory Cortex Neurons.

Sensory environments change over a wide dynamic range and sensory processing can change rapidly to facilitate stable perception. While rapid changes may occur throughout the sensory processing pathway, cortical changes are believed to profoundly influence perception. Prior stimulation studies showed that orbitofrontal cortex (OFC) can modify receptive fields and sensory coding in A1, but the engagement of OFC during listening and the pathways mediating OFC influences on A1 are unknown. We show in mice that OFC neurons respond to sounds consistent with a role of OFC in audition. We then show in vitro that OFC axons are present in A1 and excite pyramidal and GABAergic cells in all layers of A1 via glutamatergic synapses. Optogenetic stimulation of OFC terminals in A1 in vivo evokes short-latency neural activity in A1 and pairing activation of OFC projections in A1 with sounds alters sound-evoked A1 responses. Together, our results identify a direct connection from OFC to A1 that can excite A1 neurons at the earliest stage of cortical processing, and thereby sculpt A1 receptive fields. These results are consistent with a role for OFC in adjusting to changing behavioral relevance of sensory inputs and modulating A1 receptive fields to enhance sound processing.

Temporal coherence structure rapidly shapes neuronal interactions.

Perception of segregated sources is essential in navigating cluttered acoustic environments. A basic mechanism to implement this process is the temporal coherence principle. It postulates that a signal is perceived as emitted from a single source only when all of its features are temporally modulated coherently, causing them to bind perceptually. Here we report on neural correlates of this process as rapidly reshaped interactions in primary auditory cortex, measured in three different ways: as changes in response rates, as adaptations of spectrotemporal receptive fields following stimulation by temporally coherent and incoherent tone sequences, and as changes in spiking correlations during the tone sequences. Responses, sensitivity and presumed connectivity were rapidly enhanced by synchronous stimuli, and suppressed by alternating (asynchronous) sounds, but only when the animals engaged in task performance and were attentive to the stimuli. Temporal coherence and attention are therefore both important factors in auditory scene analysis.

Relative salience of spectral and temporal features in auditory long-term memory.

In order to explore the representation of sound features in auditory long-term memory, two groups of ferrets were trained on Go vs Nogo, 3-zone classification tasks. The sound stimuli differed primarily along the spectral and temporal dimensions. In Group 1, two ferrets were trained to (i) classify tones based on their frequency (Tone-task), and subsequently learned to (ii) classify white noise based on its amplitude modulation rate (AM-task). In Group 2, two ferrets were trained to classify tones based on correlated combinations of their frequency and AM rate (AM-Tone task). Both groups of ferrets learned their tasks and were able to generalize performance along the trained spectral (tone frequency) or temporal (AM rate) dimensions. Insights into stimulus representations in memory were gained when the animals were tested with a diverse set of untrained probes that mixed features from the two dimensions. Animals exhibited a complex pattern of responses to the probes reflecting primarily the probes' spectral similarity with the training stimuli, and secondarily the temporal features of the stimuli. These diverse behavioral decisions could be well accounted for by a nearest-neighbor classifier model that relied on a multiscale spectrotemporal cortical representation of the training and probe sounds.

Monkey׳s short-term auditory memory nearly abolished by combined removal of the rostral superior temporal gyrus and rhinal cortices.

While monkeys easily acquire the rules for performing visual and tactile delayed matching-to-sample, a method for testing recognition memory, they have extraordinary difficulty acquiring a similar rule in audition. Another striking difference between the modalities is that whereas bilateral ablation of the rhinal cortex (RhC) leads to profound impairment in visual and tactile recognition, the same lesion has no detectable effect on auditory recognition memory (Fritz et al., 2005). In our previous study, a mild impairment in auditory memory was obtained following bilateral ablation of the entire medial temporal lobe (MTL), including the RhC, and an equally mild effect was observed after bilateral ablation of the auditory cortical areas in the rostral superior temporal gyrus (rSTG). In order to test the hypothesis that each of these mild impairments was due to partial disconnection of acoustic input to a common target (e.g., the ventromedial prefrontal cortex), in the current study we examined the effects of a more complete auditory disconnection of this common target by combining the removals of both the rSTG and the MTL. We found that the combined lesion led to forgetting thresholds (performance at 75% accuracy) that fell precipitously from the normal retention duration of ~30 to 40s to a duration of ~1 to 2s, thus nearly abolishing auditory recognition memory, and leaving behind only a residual echoic memory. This article is part of a Special Issue entitled SI: Auditory working memory.

Mechanisms of noise robust representation of speech in primary auditory cortex.

Humans and animals can reliably perceive behaviorally relevant sounds in noisy and reverberant environments, yet the neural mechanisms behind this phenomenon are largely unknown. To understand how neural circuits represent degraded auditory stimuli with additive and reverberant distortions, we compared single-neuron responses in ferret primary auditory cortex to speech and vocalizations in four conditions: clean, additive white and pink (1/f) noise, and reverberation. Despite substantial distortion, responses of neurons to the vocalization signal remained stable, maintaining the same statistical distribution in all conditions. Stimulus spectrograms reconstructed from population responses to the distorted stimuli resembled more the original clean than the distorted signals. To explore mechanisms contributing to this robustness, we simulated neural responses using several spectrotemporal receptive field models that incorporated either a static nonlinearity or subtractive synaptic depression and multiplicative gain normalization. The static model failed to suppress the distortions. A dynamic model incorporating feed-forward synaptic depression could account for the reduction of additive noise, but only the combined model with feedback gain normalization was able to predict the effects across both additive and reverberant conditions. Thus, both mechanisms can contribute to the abilities of humans and animals to extract relevant sounds in diverse noisy environments.

Emergent selectivity for task-relevant stimuli in higher-order auditory cortex.

A variety of attention-related effects have been demonstrated in primary auditory cortex (A1). However, an understanding of the functional role of higher auditory cortical areas in guiding attention to acoustic stimuli has been elusive. We recorded from neurons in two tonotopic cortical belt areas in the dorsal posterior ectosylvian gyrus (dPEG) of ferrets trained on a simple auditory discrimination task. Neurons in dPEG showed similar basic auditory tuning properties to A1, but during behavior we observed marked differences between these areas. In the belt areas, changes in neuronal firing rate and response dynamics greatly enhanced responses to target stimuli relative to distractors, allowing for greater attentional selection during active listening. Consistent with existing anatomical evidence, the pattern of sensory tuning and behavioral modulation in auditory belt cortex links the spectrotemporal representation of the whole acoustic scene in A1 to a more abstracted representation of task-relevant stimuli observed in frontal cortex.

Rapid spectrotemporal plasticity in primary auditory cortex during behavior.

Complex natural and environmental sounds, such as speech and music, convey information along both spectral and temporal dimensions. The cortical representation of such stimuli rapidly adapts when animals become actively engaged in discriminating them. In this study, we examine the nature of these changes using simplified spectrotemporal versions (upward vs downward shifting tone sequences) with domestic ferrets (Mustela putorius). Cortical processing rapidly adapted to enhance the contrast between the two discriminated stimulus categories, by changing spectrotemporal receptive field properties to encode both the spectral and temporal structure of the tone sequences. Furthermore, the valence of the changes was closely linked to the task reward structure: stimuli associated with negative reward became enhanced relative to those associated with positive reward. These task- and-stimulus-related spectrotemporal receptive field changes occurred only in trained animals during, and immediately following, behavior. This plasticity was independently confirmed by parallel changes in a directionality function measured from the responses to the transition of tone sequences during task performance. The results demonstrate that induced patterns of rapid plasticity reflect closely the spectrotemporal structure of the task stimuli, thus extending the functional relevance of rapid task-related plasticity to the perception and learning of natural sounds such speech and animal vocalizations.

Task reward structure shapes rapid receptive field plasticity in auditory cortex.

As sensory stimuli and behavioral demands change, the attentive brain quickly identifies task-relevant stimuli and associates them with appropriate motor responses. The effects of attention on sensory processing vary across task paradigms, suggesting that the brain may use multiple strategies and mechanisms to highlight attended stimuli and link them to motor action. To better understand factors that contribute to these variable effects, we studied sensory representations in primary auditory cortex (A1) during two instrumental tasks that shared the same auditory discrimination but required different behavioral responses, either approach or avoidance. In the approach task, ferrets were rewarded for licking a spout when they heard a target tone amid a sequence of reference noise sounds. In the avoidance task, they were punished unless they inhibited licking to the target. To explore how these changes in task reward structure influenced attention-driven rapid plasticity in A1, we measured changes in sensory neural responses during behavior. Responses to the target changed selectively during both tasks but did so with opposite sign. Despite the differences in sign, both effects were consistent with a general neural coding strategy that maximizes discriminability between sound classes. The dependence of the direction of plasticity on task suggests that representations in A1 change not only to sharpen representations of task-relevant stimuli but also to amplify responses to stimuli that signal aversive outcomes and lead to behavioral inhibition. Thus, top-down control of sensory processing can be shaped by task reward structure in addition to the required sensory discrimination.

Adaptive, behaviorally gated, persistent encoding of task-relevant auditory information in ferret frontal cortex.

Top-down signals from frontal cortex are thought to be important in cognitive control of sensory processing. To explore this interaction, we compared activity in ferret frontal cortex and primary auditory cortex (A1) during auditory and visual tasks requiring discrimination between classes of reference and target stimuli. Frontal cortex responses were behaviorally gated, selectively encoded the timing and invariant behavioral meaning of target stimuli, could be rapid in onset, and sometimes persisted for hours following behavior. These results are consistent with earlier findings in A1 that attention triggered rapid, selective, persistent, task-related changes in spectrotemporal receptive fields. Simultaneously recorded local field potentials revealed behaviorally gated changes in inter-areal coherence that were selectively modulated between frontal cortex and focal regions of A1 that were responsive to target sounds. These results suggest that A1 and frontal cortex dynamically establish a functional connection during auditory behavior that shapes the flow of sensory information and maintains a persistent trace of recent task-relevant stimulus features.

Do ferrets perceive relative pitch?

The existence of relative pitch perception in animals is difficult to demonstrate, since unlike humans, animals often attend to absolute rather than relative properties of sound elements. However, the results of the present study show that ferrets can be trained using relative pitch to discriminate two-tone sequences (rising vs. falling). Three ferrets were trained using a positive-reinforcement paradigm in which sequences of reference (one to five repeats) and target stimuli were presented, and animals were rewarded only when responding correctly to the target. The training procedure consisted of three training phases that successively shaped the ferrets to attend to relative pitch. In Phase-1 training, animals learned the basic task with sequences of invariant tone-pairs and could use absolute pitch information. During Phase-2 training, in order to emphasize relative cues, absolute pitch was varied each trial within a two-octave frequency range. In Phase-3 training, absolute pitch cues were removed, and only relative cue information was available to solve the task. Two ferrets successfully completed training on all three phases and achieved significant discriminative performance over the trained four-octave frequency range. These results suggest that ferrets can be trained to discern the relative pitch relationship of a sequence of tone-pairs independent of frequency.