Humans mimicking animals: a cortical hierarchy for human vocal communication sounds.

Numerous species possess cortical regions that are most sensitive to vocalizations produced by their own kind (conspecifics). In humans, the superior temporal sulci (STSs) putatively represent homologous voice-sensitive areas of cortex. However, superior temporal sulcus (STS) regions have recently been reported to represent auditory experience or "expertise" in general rather than showing exclusive sensitivity to human vocalizations per se. Using functional magnetic resonance imaging and a unique non-stereotypical category of complex human non-verbal vocalizations-human-mimicked versions of animal vocalizations-we found a cortical hierarchy in humans optimized for processing meaningful conspecific utterances. This left-lateralized hierarchy originated near primary auditory cortices and progressed into traditional speech-sensitive areas. Our results suggest that the cortical regions supporting vocalization perception are initially organized by sensitivity to the human vocal tract in stages before the STS. Additionally, these findings have implications for the developmental time course of conspecific vocalization processing in humans as well as its evolutionary origins.

The common neural bases between sexual desire and love: a multilevel kernel density fMRI analysis.

INTRODUCTION: One of the most difficult dilemmas in relationship science and couple therapy concerns the interaction between sexual desire and love. As two mental states of intense longing for union with others, sexual desire and love are, in fact, often difficult to disentangle from one another. AIM: The present review aims to help understand the differences and similarities between these two mental states using a comprehensive statistical meta-analyses of all functional magnetic resonance imaging (fMRI) studies on sexual desire and love. METHODS: Systematic retrospective review of pertinent neuroimaging literature. MAIN OUTCOME MEASURES: Review of published literature on fMRI studies illustrating brain regions associated with love and sexual desire to date. RESULTS: Sexual desire and love not only show differences but also recruit a striking common set of brain areas that mediate somatosensory integration, reward expectation, and social cognition. More precisely, a significant posterior-to-anterior insular pattern appears to track sexual desire and love progressively. CONCLUSIONS: This specific pattern of activation suggests that love builds upon a neural circuit for emotions and pleasure, adding regions associated with reward expectancy, habit formation, and feature detection. In particular, the shared activation within the insula, with a posterior-to-anterior pattern, from desire to love, suggests that love grows out of and is a more abstract representation of the pleasant sensorimotor experiences that characterize desire. From these results, one may consider desire and love on a spectrum that evolves from integrative representations of affective visceral sensations to an ultimate representation of feelings incorporating mechanisms of reward expectancy and habit learning.

Cortical networks representing object categories and high-level attributes of familiar real-world action sounds.

In contrast to visual object processing, relatively little is known about how the human brain processes everyday real-world sounds, transforming highly complex acoustic signals into representations of meaningful events or auditory objects. We recently reported a fourfold cortical dissociation for representing action (nonvocalization) sounds correctly categorized as having been produced by human, animal, mechanical, or environmental sources. However, it was unclear how consistent those network representations were across individuals, given potential differences between each participant's degree of familiarity with the studied sounds. Moreover, it was unclear what, if any, auditory perceptual attributes might further distinguish the four conceptual sound-source categories, potentially revealing what might drive the cortical network organization for representing acoustic knowledge. Here, we used functional magnetic resonance imaging to test participants before and after extensive listening experience with action sounds, and tested for cortices that might be sensitive to each of three different high-level perceptual attributes relating to how a listener associates or interacts with the sound source. These included the sound's perceived concreteness, effectuality (ability to be affected by the listener), and spatial scale. Despite some variation of networks for environmental sounds, our results verified the stability of a fourfold dissociation of category-specific networks for real-world action sounds both before and after familiarity training. Additionally, we identified cortical regions parametrically modulated by each of the three high-level perceptual sound attributes. We propose that these attributes contribute to the network-level encoding of category-specific acoustic knowledge representations.

Cortical network differences in the sighted versus early blind for recognition of human-produced action sounds.

Both sighted and blind individuals can readily interpret meaning behind everyday real-world sounds. In sighted listeners, we previously reported that regions along the bilateral posterior superior temporal sulci (pSTS) and middle temporal gyri (pMTG) are preferentially activated when presented with recognizable action sounds. These regions have generally been hypothesized to represent primary loci for complex motion processing, including visual biological motion processing and audio-visual integration. However, it remained unclear whether, or to what degree, life-long visual experience might impact functions related to hearing perception or memory of sound-source actions. Using functional magnetic resonance imaging (fMRI), we compared brain regions activated in congenitally blind versus sighted listeners in response to hearing a wide range of recognizable human-produced action sounds (excluding vocalizations) versus unrecognized, backward-played versions of those sounds. Here, we show that recognized human action sounds commonly evoked activity in both groups along most of the left pSTS/pMTG complex, though with relatively greater activity in the right pSTS/pMTG by the blind group. These results indicate that portions of the postero-lateral temporal cortices contain domain-specific hubs for biological and/or complex motion processing independent of sensory-modality experience. Contrasting the two groups, the sighted listeners preferentially activated bilateral parietal plus medial and lateral frontal networks, whereas the blind listeners preferentially activated left anterior insula plus bilateral anterior calcarine and medial occipital regions, including what would otherwise have been visual-related cortex. These global-level network differences suggest that blind and sighted listeners may preferentially use different memory retrieval strategies when hearing and attempting to recognize action sounds.

Meta-Analyses Support a Taxonomic Model for Representations of Different Categories of Audio-Visual Interaction Events in the Human Brain.

Our ability to perceive meaningful action events involving objects, people, and other animate agents is characterized in part by an interplay of visual and auditory sensory processing and their cross-modal interactions. However, this multisensory ability can be altered or dysfunctional in some hearing and sighted individuals, and in some clinical populations. The present meta-analysis sought to test current hypotheses regarding neurobiological architectures that may mediate audio-visual multisensory processing. Reported coordinates from 82 neuroimaging studies (137 experiments) that revealed some form of audio-visual interaction in discrete brain regions were compiled, converted to a common coordinate space, and then organized along specific categorical dimensions to generate activation likelihood estimate (ALE) brain maps and various contrasts of those derived maps. The results revealed brain regions (cortical "hubs") preferentially involved in multisensory processing along different stimulus category dimensions, including 1) living versus nonliving audio-visual events, 2) audio-visual events involving vocalizations versus actions by living sources, 3) emotionally valent events, and 4) dynamic-visual versus static-visual audio-visual stimuli. These meta-analysis results are discussed in the context of neurocomputational theories of semantic knowledge representations and perception, and the brain volumes of interest are available for download to facilitate data interpretation for future neuroimaging studies.

Chinese-English bilinguals show linguistic-perceptual links in the brain associating short spoken phrases with corresponding real-world natural action sounds by semantic category.

Higher cognitive functions such as linguistic comprehension must ultimately relate to perceptual systems in the brain, though how and why this forms remains unclear. Different brain networks that mediate perception when hearing real-world natural sounds has recently been proposed to respect a taxonomic model of acoustic-semantic categories. Using functional magnetic resonance imaging (fMRI) with Chinese/English bilingual listeners, the present study explored whether reception of short spoken phrases, in both Chinese (Mandarin) and English, describing corresponding sound-producing events would engage overlapping brain regions at a semantic category level. The results revealed a double-dissociation of cortical regions that were preferential for representing knowledge of human versus environmental action events, whether conveyed through natural sounds or the corresponding spoken phrases depicted by either language. These findings of cortical hubs exhibiting linguistic-perceptual knowledge links at a semantic category level should help to advance neurocomputational models of the neurodevelopment of language systems.

Human cortical organization for processing vocalizations indicates representation of harmonic structure as a signal attribute.

The ability to detect and rapidly process harmonic sounds, which in nature are typical of animal vocalizations and speech, can be critical for communication among conspecifics and for survival. Single-unit studies have reported neurons in auditory cortex sensitive to specific combinations of frequencies (e.g., harmonics), theorized to rapidly abstract or filter for specific structures of incoming sounds, where large ensembles of such neurons may constitute spectral templates. We studied the contribution of harmonic structure to activation of putative spectral templates in human auditory cortex by using a wide variety of animal vocalizations, as well as artificially constructed iterated rippled noises (IRNs). Both the IRNs and vocalization sounds were quantitatively characterized by calculating a global harmonics-to-noise ratio (HNR). Using functional MRI, we identified HNR-sensitive regions when presenting either artificial IRNs and/or recordings of natural animal vocalizations. This activation included regions situated between functionally defined primary auditory cortices and regions preferential for processing human nonverbal vocalizations or speech sounds. These results demonstrate that the HNR of sound reflects an important second-order acoustic signal attribute that parametrically activates distinct pathways of human auditory cortex. Thus, these results provide novel support for the presence of spectral templates, which may subserve a major role in the hierarchical processing of vocalizations as a distinct category of behaviorally relevant sound.

Neuroimaging of love: fMRI meta-analysis evidence toward new perspectives in sexual medicine.

INTRODUCTION: Brain imaging is becoming a powerful tool in the study of human cerebral functions related to close personal relationships. Outside of subcortical structures traditionally thought to be involved in reward-related systems, a wide range of neuroimaging studies in relationship science indicate a prominent role for different cortical networks and cognitive factors. Thus, the field needs a better anatomical/network/whole-brain model to help translate scientific knowledge from lab bench to clinical models and ultimately to the patients suffering from disorders associated with love and couple relationships. AIM: The aim of the present review is to provide a review across wide range of functional magnetic resonance imaging (fMRI) studies to critically identify the cortical networks associated with passionate love, and to compare and contrast it with other types of love (such as maternal love and unconditional love for persons with intellectual disabilities). METHODS: Retrospective review of pertinent neuroimaging literature. MAIN OUTCOME MEASURES: Review of published literature on fMRI studies of love illustrating brain regions associated with different forms of love. RESULTS: Although all fMRI studies of love point to the subcortical dopaminergic reward-related brain systems (involving dopamine and oxytocin receptors) for motivating individuals in pair-bonding, the present meta-analysis newly demonstrated that different types of love involve distinct cerebral networks, including those for higher cognitive functions such as social cognition and bodily self-representation. CONCLUSIONS: These metaresults provide the first stages of a global neuroanatomical model of cortical networks involved in emotions related to different aspects of love. Developing this model in future studies should be helpful for advancing clinical approaches helpful in sexual medicine and couple therapy.

Processing of Real-World, Dynamic Natural Stimuli in Autism is Linked to Corticobasal Function.

Many individuals with autism spectrum disorder (ASD) have been shown to perceive everyday sensory information differently compared to peers without autism. Research examining these sensory differences has primarily utilized nonnatural stimuli or natural stimuli using static photos with few having utilized dynamic, real-world nonverbal stimuli. Therefore, in this study, we used functional magnetic resonance imaging to characterize brain activation of individuals with high-functioning autism when viewing and listening to a video of a real-world scene (a person bouncing a ball) and anticipating the bounce. We investigated both multisensory and unisensory processing and hypothesized that individuals with ASD would show differential activation in (a) primary auditory and visual sensory cortical and association areas, and in (b) cortical and subcortical regions where auditory and visual information is integrated (e.g. temporal-parietal junction, pulvinar, superior colliculus). Contrary to our hypotheses, the whole-brain analysis revealed similar activation between the groups in these brain regions. However, compared to controls the ASD group showed significant hypoactivation in the left intraparietal sulcus and left putamen/globus pallidus. We theorize that this hypoactivation reflected underconnectivity for mediating spatiotemporal processing of the visual biological motion stimuli with the task demands of anticipating the timing of the bounce event. The paradigm thus may have tapped into a specific left-lateralized aberrant corticobasal circuit or loop involved in initiating or inhibiting motor responses. This was consistent with a dual "when versus where" psychophysical model of corticobasal function, which may reflect core differences in sensory processing of real-world, nonverbal natural stimuli in ASD. Autism Res 2020, 13: 539-549. © 2020 International Society for Autism Research, Wiley Periodicals, Inc. LAY SUMMARY: To understand how individuals with autism perceive the real-world, using magnetic resonance imaging we examined brain activation in individuals with autism while watching a video of someone bouncing a basketball. Those with autism had similar activation to controls in auditory and visual sensory brain regions, but less activation in an area that processes information about body movements and in a region involved in modulating movements. These areas are important for understanding the actions of others and developing social skills.

Electrophysiological Evidence of Early Cortical Sensitivity to Human Conspecific Mimic Voice as a Distinct Category of Natural Sound.

Purpose From an anthropological perspective of hominin communication, the human auditory system likely evolved to enable special sensitivity to sounds produced by the vocal tracts of human conspecifics whether attended or passively heard. While numerous electrophysiological studies have used stereotypical human-produced verbal (speech voice and singing voice) and nonverbal vocalizations to identify human voice-sensitive responses, controversy remains as to when (and where) processing of acoustic signal attributes characteristic of "human voiceness" per se initiate in the brain. Method To explore this, we used animal vocalizations and human-mimicked versions of those calls ("mimic voice") to examine late auditory evoked potential responses in humans. Results Here, we revealed an N1b component (96-120 ms poststimulus) during a nonattending listening condition showing significantly greater magnitude in response to mimics, beginning as early as primary auditory cortices, preceding the time window reported in previous studies that revealed species-specific vocalization processing initiating in the range of 147-219 ms. During a sound discrimination task, a P600 (500-700 ms poststimulus) component showed specificity for accurate discrimination of human mimic voice. Distinct acoustic signal attributes and features of the stimuli were used in a classifier model, which could distinguish most human from animal voice comparably to behavioral data-though none of these single features could adequately distinguish human voiceness. Conclusions These results provide novel ideas for algorithms used in neuromimetic hearing aids, as well as direct electrophysiological support for a neurocognitive model of natural sound processing that informs both neurodevelopmental and anthropological models regarding the establishment of auditory communication systems in humans. Supplemental Material https://doi.org/10.23641/asha.12903839.

Different categories of living and non-living sound-sources activate distinct cortical networks.

With regard to hearing perception, it remains unclear as to whether, or the extent to which, different conceptual categories of real-world sounds and related categorical knowledge are differentially represented in the brain. Semantic knowledge representations are reported to include the major divisions of living versus non-living things, plus more specific categories including animals, tools, biological motion, faces, and places-categories typically defined by their characteristic visual features. Here, we used functional magnetic resonance imaging (fMRI) to identify brain regions showing preferential activity to four categories of action sounds, which included non-vocal human and animal actions (living), plus mechanical and environmental sound-producing actions (non-living). The results showed a striking antero-posterior division in cortical representations for sounds produced by living versus non-living sources. Additionally, there were several significant differences by category, depending on whether the task was category-specific (e.g. human or not) versus non-specific (detect end-of-sound). In general, (1) human-produced sounds yielded robust activation in the bilateral posterior superior temporal sulci independent of task. Task demands modulated activation of left lateralized fronto-parietal regions, bilateral insular cortices, and sub-cortical regions previously implicated in observation-execution matching, consistent with "embodied" and mirror-neuron network representations subserving recognition. (2) Animal action sounds preferentially activated the bilateral posterior insulae. (3) Mechanical sounds activated the anterior superior temporal gyri and parahippocampal cortices. (4) Environmental sounds preferentially activated dorsal occipital and medial parietal cortices. Overall, this multi-level dissociation of networks for preferentially representing distinct sound-source categories provides novel support for grounded cognition models that may underlie organizational principles for hearing perception.

Breastfeeding Duration Is Associated with Regional, but Not Global, Differences in White Matter Tracts.

Extended breastfeeding through infancy confers benefits on neurocognitive performance and intelligence tests, though few have examined the biological basis of these effects. To investigate correlations with breastfeeding, we examined the major white matter tracts in 4-8 year-old children using diffusion tensor imaging and volumetric measurements of the corpus callosum. We found a significant correlation between the duration of infant breastfeeding and fractional anisotropy scores in left-lateralized white matter tracts, including the left superior longitudinal fasciculus and left angular bundle, which is indicative of greater intrahemispheric connectivity. However, in contrast to expectations from earlier studies, no correlations were observed with corpus callosum size, and thus no correlations were observed when using such measures of global interhemispheric white matter connectivity development. These findings suggest a complex but significant positive association between breastfeeding duration and white matter connectivity, including in pathways known to be functionally relevant for reading and language development.

Hearing and orally mimicking different acoustic-semantic categories of natural sound engage distinct left hemisphere cortical regions.

Oral mimicry is thought to represent an essential process for the neurodevelopment of spoken language systems in infants, the evolution of language in hominins, and a process that could possibly aid recovery in stroke patients. Using functional magnetic resonance imaging (fMRI), we previously reported a divergence of auditory cortical pathways mediating perception of specific categories of natural sounds. However, it remained unclear if or how this fundamental sensory organization by the brain might relate to motor output, such as sound mimicry. Here, using fMRI, we revealed a dissociation of activated brain regions preferential for hearing with the intent to imitate and the oral mimicry of animal action sounds versus animal vocalizations as distinct acoustic-semantic categories. This functional dissociation may reflect components of a rudimentary cortical architecture that links systems for processing acoustic-semantic universals of natural sound with motor-related systems mediating oral mimicry at a category level. The observation of different brain regions involved in different aspects of oral mimicry may inform targeted therapies for rehabilitation of functional abilities after stroke.

Divergent Human Cortical Regions for Processing Distinct Acoustic-Semantic Categories of Natural Sounds: Animal Action Sounds vs. Vocalizations.

A major gap in our understanding of natural sound processing is knowledge of where or how in a cortical hierarchy differential processing leads to categorical perception at a semantic level. Here, using functional magnetic resonance imaging (fMRI) we sought to determine if and where cortical pathways in humans might diverge for processing action sounds vs. vocalizations as distinct acoustic-semantic categories of real-world sound when matched for duration and intensity. This was tested by using relatively less semantically complex natural sounds produced by non-conspecific animals rather than humans. Our results revealed a striking double-dissociation of activated networks bilaterally. This included a previously well described pathway preferential for processing vocalization signals directed laterally from functionally defined primary auditory cortices to the anterior superior temporal gyri, and a less well-described pathway preferential for processing animal action sounds directed medially to the posterior insulae. We additionally found that some of these regions and associated cortical networks showed parametric sensitivity to high-order quantifiable acoustic signal attributes and/or to perceptual features of the natural stimuli, such as the degree of perceived recognition or intentional understanding. Overall, these results supported a neurobiological theoretical framework for how the mammalian brain may be fundamentally organized to process acoustically and acoustic-semantically distinct categories of ethologically valid, real-world sounds.

A quantitative meta-analysis of functional imaging studies of social rejection.

Early neuroimaging studies using Cyberball suggested that social rejection activated the pain matrix, as identified in studies of physical pain. However, these early studies were characterized by small sample sizes. Our statistical multi-level kernel density analysis (MKDA) of Cyberball neuroimaging studies with 244 participants fails to support the claim that social rejection operates on the same pain matrix as nociceptive stimuli, questioning whether social pain is more figurative or literal. We also performed an MKDA of the neuroimaging studies of reliving a romantic rejection to test whether the pain matrix was activated if the rejection were more meaningful. Results again failed to support the notion that rejection activates the neural matrix identified in studies of physical pain. Reliving an unwanted rejection by a romantic partner was significantly characterized by activation within and beyond the "Cyberball" brain network, suggesting that the neural correlates of social pain are more complex than previously thought.

Beyond human intentions and emotions.

Although significant advances have been made in our understanding of the neural basis of action observation and intention understanding in the last few decades by studies demonstrating the involvement of a specific brain network (action observation network; AON), these have been largely based on experimental studies in which people have been considered as strictly isolated entities. However, we, as social species, spend much more of our time performing actions interacting with others. Research shows that a person's position along the continuum of perceived social isolation/bonding to others is associated with a variety of physical and mental health effects. Thus, there is a crucial need to better understand the neural basis of intention understanding performed in interpersonal and emotional contexts. To address this issue, we performed a meta-analysis using of functional magnetic resonance imaging (fMRI) studies over the past decade that examined brain and cortical network processing associated with understanding the intention of others actions vs. those associated with passionate love for others. Both overlapping and distinct cortical and subcortical regions were identified for intention and love, respectively. These findings provide scientists and clinicians with a set of brain regions that can be targeted for future neuroscientific studies on intention understanding, and help develop neurocognitive models of pair-bonding.

Selective decision-making deficit in love following damage to the anterior insula.

Neuroimaging studies have found a correlation between activation in the anterior insula and love, and a correlation between activation in the posterior insula and lust. The present control-case study describes a neurological male patient, with a rare, circumscribed lesion in the anterior insula, whom we tested using a decision task that required he judge whether each of a series of attractive individuals could be the object of his love or lust. The patient, in contrast with neurologically typical participants matched on age, gender, and ethnicity, performed normally when making decisions about lust but showed a selective deficit when making decisions about love. These results provide the first clinical evidence indicating that the anterior insula may play an instrumental role in love but not lust more generally. These data support the notion of a posterior-to-anterior insular gradient, from sensorimotor to abstract representations, in the evaluation of anticipatory rewards in interpersonal relationships.

Auditory object salience: human cortical processing of non-biological action sounds and their acoustic signal attributes.

Whether viewed or heard, an object in action can be segmented as a distinct salient event based on a number of different sensory cues. In the visual system, several low-level attributes of an image are processed along parallel hierarchies, involving intermediate stages wherein gross-level object form and/or motion features are extracted prior to stages that show greater specificity for different object categories (e.g., people, buildings, or tools). In the auditory system, though relying on a rather different set of low-level signal attributes, meaningful real-world acoustic events and "auditory objects" can also be readily distinguished from background scenes. However, the nature of the acoustic signal attributes or gross-level perceptual features that may be explicitly processed along intermediate cortical processing stages remain poorly understood. Examining mechanical and environmental action sounds, representing two distinct non-biological categories of action sources, we had participants assess the degree to which each sound was perceived as object-like versus scene-like. We re-analyzed data from two of our earlier functional magnetic resonance imaging (fMRI) task paradigms (Engel et al., 2009) and found that scene-like action sounds preferentially led to activation along several midline cortical structures, but with strong dependence on listening task demands. In contrast, bilateral foci along the superior temporal gyri (STG) showed parametrically increasing activation to action sounds rated as more "object-like," independent of sound category or task demands. Moreover, these STG regions also showed parametric sensitivity to spectral structure variations (SSVs) of the action sounds-a quantitative measure of change in entropy of the acoustic signals over time-and the right STG additionally showed parametric sensitivity to measures of mean entropy and harmonic content of the environmental sounds. Analogous to the visual system, intermediate stages of the auditory system appear to process or extract a number of quantifiable low-order signal attributes that are characteristic of action events perceived as being object-like, representing stages that may begin to dissociate different perceptual dimensions and categories of every-day, real-world action sounds.