The cerebral cortex is a major hub for the convergence and integration of signals from across the sensory modalities; sensory cortices, including primary regions, are no exception. Here we show that visual stimuli influence neural firing in the auditory cortex of awake male and female mice, using multisite probes to sample single units across multiple cortical layers. We demonstrate that visual stimuli influence firing in both primary and secondary auditory cortex. We then determine the laminar location of recording sites through electrode track tracing with fluorescent dye and optogenetic identification using layer-specific markers. Spiking responses to visual stimulation occur deep in auditory cortex and are particularly prominent in layer 6. Visual modulation of firing rate occurs more frequently at areas with secondary-like auditory responses than those with primary-like responses. Auditory cortical responses to drifting visual gratings are not orientation-tuned, unlike visual cortex responses. The deepest cortical layers thus appear to be an important locus for cross-modal integration in auditory cortex. The deepest layers of the auditory cortex are often considered its most enigmatic, possessing a wide range of cell morphologies and atypical sensory responses. Here we show that, in mouse auditory cortex, these layers represent a locus of cross-modal convergence, containing many units responsive to visual stimuli. Our results suggest that this visual signal conveys the presence and timing of a stimulus rather than specifics about that stimulus, such as its orientation. These results shed light on both how and what types of cross-modal information is integrated at the earliest stages of sensory cortical processing.

Visual Abstract

Across all languages studied to date, audiovisual speech exhibits a consistent rhythmic structure. This rhythm is critical to speech perception. Some have suggested that the speech rhythm evolved de novo in humans. An alternative account—the one we explored here—is that the rhythm of speech evolved through the modification of rhythmic facial expressions. We tested this idea by investigating the structure and development of macaque monkey lipsmacks and found that their developmental trajectory is strikingly similar to the one that leads from human infant babbling to adult speech. Specifically, we show that: 1) younger monkeys produce slower, more variable mouth movements and as they get older, these movements become faster and less variable; and 2) this developmental pattern does not occur for another cyclical mouth movement—chewing. These patterns parallel human developmental patterns for speech and chewing. They suggest that, in both species, the two types of rhythmic mouth movements use different underlying neural circuits that develop in different ways. Ultimately, both lipsmacking and speech converge on a ~5 Hz rhythm that represents the frequency that characterizes the speech rhythm of human adults. We conclude that monkey lipsmacking and human speech share a homologous developmental mechanism, lending strong empirical support for the idea that the human speech rhythm evolved from the rhythmic facial expressions of our primate ancestors.

Human speech universally exhibits a 3-to 8-Hz rhythm, corresponding to the rate of syllable production, which is reflected in both the sound envelope and the visual mouth movements. Artificial perturbation of the speech rhythm outside the natural range reduces speech intelligibility, demonstrating a perceptual tuning to this frequency band. One theory posits that the mouth movements at the core of this speech rhythm evolved through modification of ancestral primate facial expressions. Recent evidence shows that one such communicative gesture in macaque monkeys, lip-smacking, has motor parallels with speech in its rhythmicity, its developmental trajectory, and the coordination of vocal tract structures. Whether monkeys also exhibit a perceptual tuning to the natural rhythms of lip-smacking is unknown. To investigate this, we tested rhesus monkeys in a preferential-looking procedure, measuring the time spent looking at each of two side-by-side computer-generated monkey avatars lip-smacking at natural versus sped-up or sloweddown rhythms. Monkeys showed an overall preference for the natural rhythm compared with the perturbed rhythms. This lends behavioral support for the hypothesis that perceptual processes in monkeys are similarly tuned to the natural frequencies of communication signals as they are in humans. Our data provide perceptual evidence for the theory that speech may have evolved from ancestral primate rhythmic facial expressions.

Audiovisual speech has a stereotypical rhythm that is between 2 and 7 Hz, and deviations from this frequency range in either modality reduce intelligibility. Understanding how audiovisual speech evolved requires investigating the origins of this rhythmic structure. One hypothesis is that the rhythm of speech evolved through the modification of some pre-existing cyclical jaw movements in a primate ancestor. We tested this hypothesis by investigating the temporal structure of lipsmacks and teeth-grinds of macaque monkeys and the neural responses to these facial gestures in the superior temporal sulcus (STS), a region implicated in the processing of audiovisual communication signals in both humans and monkeys. We found that both lipsmacks and teeth-grinds have consistent but distinct peak frequencies and that both fall well within the 2–7 Hz range of mouth movements associated with audiovisual speech. Single neurons and local field potentials of the STS of monkeys readily responded to such facial rhythms, but also responded just as robustly to yawns, a nonrhythmic but dynamic facial expression. All expressions elicited enhanced power in the delta (0–3Hz), theta (3–8Hz), alpha (8–14Hz) and gamma (> 60 Hz) frequency ranges, and suppressed power in the beta (20–40Hz) range. Thus, STS is sensitive to, but not selective for, rhythmic facial gestures. Taken together, these data provide support for the idea that that audiovisual speech evolved (at least in part) from the rhythmic facial gestures of an ancestral primate and that the STS was sensitive to and thus ‘prepared’ for the advent of rhythmic audiovisual communication.

Noisy acoustic environments present several challenges for the evolution of acoustic communication systems. Among the most significant is the need to limit degradation of spectro-temporal signal structure in order to maintain communicative efficacy. This can be achieved by selecting for several potentially complementary processes. Selection can act on behavioral mechanisms permitting signalers to control the timing and occurrence of signal production to avoid acoustic interference. Likewise, the signal itself may be the target of selection, biasing the evolution of its structure to comprise acoustic features that avoid interference from ambient noise or degrade minimally in the habitat. Here, we address the latter topic for common marmoset (Callithrix jacchus) long-distance contact vocalizations, known as phee calls. Our aim was to test whether this vocalization is specifically adapted for transmission in a species-typical forest habitat, the Atlantic forests of northeastern Brazil. We combined seasonal analyses of ambient habitat acoustics with experiments in which pure tones, clicks, and vocalizations were broadcast and rerecorded at different distances to characterize signal degradation in the habitat. Ambient sound was analyzed from intervals throughout the day and over rainy and dry seasons, showing temporal regularities across varied timescales. Broadcast experiment results indicated that the tone and click stimuli showed the typically inverse relationship between frequency and signaling efficacy. Although marmoset phee calls degraded over distance with marked predictability compared with artificial sounds, they did not otherwise appear to be specially designed for increased transmission efficacy or minimal interference in this habitat. We discuss these data in the context of other similar studies and evidence of potential behavioral mechanisms for avoiding acoustic interference in order to maintain effective vocal communication in common marmosets.

A common pattern in dominance hierarchies is that some ranks result in higher levels of psychosocial stress than others. Such stress can lead to negative health outcomes, possibly through altered levels of stress hormones. The dominance rank-stress physiology relationship is known to vary between species; sometimes dominants show higher levels of glucocorticoid stress hormones, whereas in other cases subordinates show higher levels. It is less clear how this relationship varies between groups of different ages or cultures. In this study, we used long-term cortisol measurement methods to compare the effect of rank on cortisol levels in adult and adolescent male rhesus macaques. In the adult groups, subordinates had significantly higher cortisol levels. In the adolescents, no significant correlation between cortisol and status was found. Further analysis demonstrated that the adult hierarchy was stricter than that of the adolescents. Adult subordinates received extreme aggression more frequently than dominants, and this class of behavior was positively correlated with cortisol; by contrast, adolescents showed neither trend. Together, these findings provide evidence for a cortisol-rank relationship determined by social factors, namely, despotism of the group, and highlight the importance of group-specific social analysis when comparing or combining results obtained from different groups of animals.

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