Auditory and visual systems organization in Brodmann Area 8 for gaze-shift control: where we do not see, we can hear

Hearing is especially important for most primate species as they live in habitats of dense vegetation that limits vision. Stebbins (1980) summed up the evolution of the auditory system by assuming that earliest mammals exploited nocturnal niches since they were relatively free of many of the large, diurnal, predacious reptiles. Therefore, hearing and smell were more useful at night than vision. Our vision is limited not only in the dark but also outside the visual field. In fact, if we observe the behavior of a predator like a feline, oriented toward its prey, and at the same time a sound occurs behind, we might note three principal different behaviors: the predator could maintain its gaze and ears on the prey neglecting the sound source; the predator could maintain its gaze on the prey rotating ears and then shifting its auditory attention toward the sound source; finally the predator could break its attention and orient gaze and ears toward the sound source. A similar behavior is seen in human beings during social interaction with two or more interlocutors. In humans, orienting movements are carried out by the eyes, head, and/or body operating alone or in various combinations depending on the behavioral situation. However, in non-human primates, such as macaque monkeys, head orienting movements and, more generally, gaze-shift are accompanied by ear orienting movements, which allow the shifting of auditory attention toward a sound of interest (Bon and Lucchetti, 1994, 2006; Lucchetti et al., 2008; Lanzilotto et al., 2013; Yin, 2013). Considering all these assumptions, the auditory system could have an important role to detect information even from regions of the space that the visual system cannot explore without orienting movements. In other words, where we cannot see, we can hear. Through this opinion article, we argue that Brodmann Area 8 receives information from both auditory and visual systems and organizes a transformation of these sensory signals into gaze-shift motor commands. Our hypothesis is that this sensory-motor transformation is spatially organized, from both anatomical and functional points of view. Anatomical and functional properties of the Brodmann Area 8 (consisting in Area 8A plus Area 8B) support a medio-lateral organization for both auditory and visual systems. In particular, the lateral portion, corresponding to Area 8A or Frontal Eye Field (FEF), could play a role in receiving visual and auditory information from a central part of the visual field and then in organizing gaze-shift motor commands toward it. Otherwise, the medial portion, corresponding to Area 8B or Premotor Ear-Eye Field (PEEF), could play a role in receiving principally auditory information from a peripheral region of the space and then in organizing gaze-shift motor commands toward it

Evidence for a functional subdivision of Premotor Ear-Eye Field (Aera 8B)

The Supplementary EyeField (SEF) and the Frontal Eye Field (FEF) have been described as participating in gaze shift control. Recent evidence suggests, however, that other areas of the dorso medial prefrontal cortex also influence gaze shift. Herein, we haveinvestigated electrically evoked ear-and eye movements from the PremotorEar-Eye Field, or PEEF (area8B) of macaque monkeys. We stimulated PEEF during spontaneous condition (outside the task performance) and during the execution of a visual fixation task(VFT). In the first case, we functionally identified two regions within the PEEF: a core and a belt. In the core region, stimulation elicited forward ear movements; regarding the evoked eye movements, in some penetrations, stimulation elicited contraversive fixed-vectors with a mean amplitude of 5.14◦; while in other penetrations, we observed prevalently contralateral goal-directed eye movements having end-points that fell within15◦ inrespect to the primary eye position. On the contrary, in the belt region,stimulation elicited backward ear movements; regarding the eye movements, in some penetrations stimulation elicited prevalently contralateral goal-directed eye movements having end-points that fell within 15◦ in respect to the primary eye position, while in the lateral edge of the investigated region, stimulation elicited contralateral goal-directedey emovements having end-points that fell beyond 15◦in respect to the primary eye position. Stimulation during VFT either did not elicit eye movements or evoked saccades of only a few degrees. Finally, even though no head rotation movements were observed during the stimulation period, we viewed a relationship between the duration of stimulation and the neck forces exerted by the monkey’shead. We propose an updated vision of the PEEF composed of two functional regions, core and belt, which may beinvolved in integrating auditory and visual information important to the programming of gaze orienting movements

Neuronal Encoding of Self and Others' Head Rotation in the Macaque Dorsal Prefrontal Cortex.

Following gaze is a crucial skill, in primates, for understanding where and at what others are looking, and often requires head rotation. The neural basis underlying head rotation are deemed to overlap with the parieto-frontal attention/gaze-shift network. Here, we show that a set of neurons in monkey's Brodmann area 9/46dr (BA 9/46dr), which is involved in orienting processes and joint attention, becomes active during self head rotation and that the activity of these neurons cannot be accounted for by saccade-related activity (head-rotation neurons). Another set of BA 9/46dr neurons encodes head rotation performed by an observed agent facing the monkey (visually triggered neurons). Among these latter neurons, almost half exhibit the intriguing property of encoding both execution and observation of head rotation (mirror-like neurons). Finally, by means of neuronal tracing techniques, we showed that BA 9/46dr takes part into two distinct networks: a dorso/mesial network, playing a role in spatial head/gaze orientation, and a ventrolateral network, likely involved in processing social stimuli and mirroring others' head. The overall results of this study provide a new, comprehensive picture of the role of BA 9/46dr in encoding self and others' head rotation, likely playing a role in head-following behaviors

Local and system mechanisms for action execution and observation in parietal and premotor cortices

The action observation network (AON) includes a system of brain areas largely shared with action execution in both human and nonhuman primates. Yet temporal and tuning specificities of distinct areas and of physiologically identified neuronal classes in the encoding of self and others’ action remain unknown. We recorded the activity of 355 single units from three crucial nodes of the AON, the anterior intraparietal area (AIP), and premotor areas F5 and F6, while monkeys performed a Go/No-Go grasping task and observed an experimenter performing it. At the system level, during task execution, F6 displays a prevalence of suppressed neurons and signals whether an action has to be performed, whereas AIP and F5 share a prevalence of facilitated neurons and remarkable target selectivity; during task observation, F5 stands out for its unique prevalence of facilitated neurons and its stronger and earlier modulation than AIP and F6. By applying unsupervised clustering of spike waveforms, we found distinct cell classes unevenly distributed across areas, with different firing properties and carrying specific visuomotor signals. Broadly spiking neurons exhibited a balanced amount of facilitated and suppressed activity during action execution and observation, whereas narrower spiking neurons showed more mutually facilitated responses during the execution of one’s own and others’ action, particularly in areas AIP and F5. Our findings elucidate the time course of activity and firing properties of neurons in the AON during one’s own and others’ action, from the system level of anatomically distinct areas to the local level of physiologically distinct cell classes

Anterior Intraparietal Area: a Hub in the Observed Manipulative Action Network.

Current knowledge regarding the processing of observed manipulative actions (OMAs) (e.g., grasping, dragging, or dropping) is limited to grasping and underlying neural circuitry remains controversial. Here, we addressed these issues by combining chronic neuronal recordings along the anteroposterior extent of monkeys\u2019 anterior intraparietal (AIP) area with tracer injections into the recorded sites. We found robust neural selectivity for 7 distinct OMAs, particularly in the posterior part of AIP (pAIP), where it was associated with motor coding of grip type and own-hand visual feedback. This cluster of functional properties appears to be specifically grounded in stronger direct connections of pAIP with the temporal regions of the ventral visual stream and the prefrontal cortex, as connections with skeletomotor related areas and regions of the dorsal visual stream exhibited opposite or no rostrocaudal gradients. Temporal and prefrontal areas may provide visual and contextual information relevant for manipulative action processing. These results revise existing models of the action observation network, suggesting that pAIP constitutes a parietal hub for routing information about OMA identity to the other nodes of the network