Monkeys and Humans Share a Common Computation for Face/Voice Integration

Speech production involves the movement of the mouth and other regions of the face resulting in visual motion cues. These visual cues enhance intelligibility and detection of auditory speech. As such, face-to-face speech is fundamentally a multisensory phenomenon. If speech is fundamentally multisensory, it should be reflected in the evolution of vocal communication: similar behavioral effects should be observed in other primates. Old World monkeys share with humans vocal production biomechanics and communicate face-to-face with vocalizations. It is unknown, however, if they, too, combine faces and voices to enhance their perception of vocalizations. We show that they do: monkeys combine faces and voices in noisy environments to enhance their detection of vocalizations. Their behavior parallels that of humans performing an identical task. We explored what common computational mechanism(s) could explain the pattern of results we observed across species. Standard explanations or models such as the principle of inverse effectiveness and a “race” model failed to account for their behavior patterns. Conversely, a “superposition model”, positing the linear summation of activity patterns in response to visual and auditory components of vocalizations, served as a straightforward but powerful explanatory mechanism for the observed behaviors in both species. As such, it represents a putative homologous mechanism for integrating faces and voices across primates

Visual responses on neck muscles reveal selective gating that prevents express Saccades

Express saccades promote the acquisition of visual targets at extremely short reaction times. Because of the head's considerable inertia, it is unknown whether express saccades are accompanied by a parallel command to the head. Here, by recording electromyographic (EMG) activity from monkey neck muscles, we demonstrate that visual target presentation elicits time-locked, lateralized recruitment of neck muscles at extremely short latencies (55-95 ms). Remarkably, such recruitment not only accompanies express saccades, but also precedes nonexpress saccades, occasionally by up to 150 ms. These results demonstrate selective gating of components of descending commands from the superior colliculus to prevent express saccades yet permit recruitment of a head orienting synergy. We conclude that such selective gating aids eye-head coordination by permitting force development at neck muscles while a decision to commit to a gaze shift is being made, optimizing the contribution of the more inertial head to the ensuing gaze shift

Neck muscle responses to stimulation of monkey superior colliculus. I. Topography and manipulation of stimulation parameters

The role of the primate superior colliculus (SC) in orienting head movements was studied by recording electromyographic (EMG) activity from multiple neck muscles following electrical stimulation of the SC. Combining SC stimulation with neck EMG recordings provides an objective and sensitive measure of the SC drive onto neck muscle motoneurons, particularly in relation to evoked gaze shifts. In this paper, we address how neck EMG responses to SC stimulation in head-restrained monkeys depend on the rostrocaudal, mediolateral, and dorsoventral location of the stimulating electrode within the SC and vary with manipulations of the eye position prior to stimulation onset and changes in stimulation current and duration. Stimulation predominantly evoked EMG responses on the muscles obliquus capitis inferior, rectus capitis posterior major, and splenius capitis. These responses became larger in magnitude and shorter in onset latency for progressively more caudal stimulation locations, consistent with turning the head. However, evoked responses persisted even for more rostral stimulation locations usually not associated with head movements. Manipulating initial eye position revealed that the magnitude of evoked responses became stronger as the eyes attained positions contralateral to the side of stimulation, consistent with a summation between a generic command evoked by SC stimulation and the influence of eye position on tonic neck EMG. Manipulating stimulation current and duration revealed that the relationship between gaze shifts and evoked EMG responses is not obligatory: short-duration (150 ms) occasionally revealed a transient neck EMG response aligned on the onset of sequential gaze shifts. We conclude that the SC drive to neck muscle motoneurons is far more widespread than traditionally supposed and is relayed through intervening elements which may or may not be activated in association with gaze shifts

The influence of stimulus properties on multisensory processing in the awake primate superior colliculus.

Multisensory integration is a process whereby information converges from different sensory modalities to produce a response that is different from that elicited by the individual modalities presented alone. A neural basis for multisensory integration has been identified within a variety of brain regions, but the most thoroughly examined model has been that of the superior colliculus (SC). Multisensory processing in the SC of anaesthetized animals has been shown to be dependent on the physical parameters of the individual stimuli presented (e.g., intensity, direction, velocity) as well as their spatial relationship. However, it is unknown whether these stimulus features are important, or evident, in the awake behaving animal. To address this question, we evaluated the influence of physical properties of sensory stimuli (visual intensity, direction, and velocity; auditory intensity and location) on sensory activity and multisensory integration of SC neurons in awake, behaving primates. Monkeys were trained to fixate a central visual fixation point while visual and/or auditory stimuli were presented in the periphery. Visual stimuli were always presented within the contralateral receptive field of the neuron whereas auditory stimuli were presented at either ipsi- or contralateral locations. Many of the SC neurons responsive to these sensory stimuli (n = 66/84; 76%) had stronger responses when the visual and auditory stimuli were combined at contralateral locations than when the auditory stimulus was located on the ipsilateral side. This trend was significant across the population of auditory-responsive neurons. In addition, some SC neurons (n = 31) were presented a battery of tests in which the quality of one stimulus of a pair was systematically manipulated. A small proportion of these neurons (n = 8/31; 26%) showed preferential responses to stimuli with specific physical properties, and these preferences were not significantly altered when multisensory stimulus combinations were presented. These data demonstrate that multisensory processing in the awake behaving primate is influenced by the spatial congruency of the stimuli as well as their individual physical properties

Engagement of visual fixation suppresses sensory responsiveness and multisensory integration in the primate superior colliculus.

Neurons in the intermediate and deep layers of the superior colliculus (SC) often exhibit sensory-related activity in addition to discharging for saccadic eye movements. These two patterns of activity can combine so that modifications of the sensory response can lead to changes in orienting behaviour. Can behavioural factors, however, influence sensory activity? In this study of rhesus monkeys, we isolate one behavioural factor, the state of visual fixation, and examine its influences on sensory processing and multisensory integration in the primate SC. Two interleaved fixation conditions were used: a FIX condition requiring exogenous fixation of a visible fixation point; and a FIX-BLINK condition, requiring endogenous fixation in the absence of a visible fixation point. Neurons of the SC were influenced by fixation state, exhibiting both lower levels of sensory activity and reduced multisensory interactions when fixation was exogenously engaged on a visible fixation point. These results are consistent with active visual fixation suppressing responses to extraneous stimuli, and thus demonstrate that sensory processing and multisensory responses in the SC are not dependent solely on the physical properties of the sensory environment, but are also dynamically influenced by the behavioural state of the animal

Neck muscles in the rhesus monkey. II. Electromyographic patterns of activation underlying postures and movements

Electromyographic (EMG) activity was recorded in less than or equal to 12 neck muscles in four alert monkeys whose heads were unrestrained to describe the spatial and temporal patterns of neck muscle activation accompanying a large range of head postures and movements. Some head postures and movements were elicited by training animals to generate gaze shifts to visual targets. Other spontaneous head movements were made during orienting, tracking, feeding, expressive, and head-shaking behaviors. These latter movements exhibited a wider range of kinematic patterns. Stable postures and small head movements of only a few degrees were associated with activation of a small number of muscles in a reproducible synergy. Additional muscles were recruited for more eccentric postures and larger movements. For head movements during trained gaze shifts, movement amplitude, velocity, and acceleration were correlated linearly and agonist muscles were recruited without antagonist muscles. Complex sequences of reciprocal bursts in agonist and antagonist muscles were observed during very brisk movements. Turning movements of similar amplitudes that began from different initial head positions were associated with systematic variations in the activities of different muscles and in the relative timings of these activities. Unique recruitment synergies were observed during feeding and head-shaking behaviors. Our results emphasize that the recruitment of a given muscle was generally ordered and consistent but that strategies for coordination among various neck muscles were often complex and appeared to depend on the specifics of musculoskeletal architecture, posture, and movement kinematics that differ substantially among species