Aihua Chen

Macaque Parieto-Insular Vestibular Cortex: Responses to Self-Motion and Optic Flow

The parieto-insular vestibular cortex (PIVC) is thought to contain an important representation of vestibular information. Here we describe responses of macaque PIVC neurons to three-dimensional (3D) vestibular and optic flow stimulation. We found robust vestibular responses to both translational and rotational stimuli in the retroinsular (Ri) and adjacent secondary somatosensory (S2) cortices. PIVC neurons did not respond to optic flow stimulation, and vestibular responses were similar in darkness and during visual fixation. Cells in the upper bank and tip of the lateral sulcus (Ri and S2) responded to sinusoidal vestibular stimuli with modulation at the first harmonic frequency and were directionally tuned. Cells in the lower bank of the lateral sulcus (mostly Ri) often modulated at the second harmonic frequency and showed either bimodal spatial tuning or no tuning at all. All directions of 3D motion were represented in PIVC, with direction preferences distributed approximately uniformly for translation, but showing a preference for roll rotation. Spatiotemporal profiles of responses to translation revealed that half of PIVC cells followed the linear velocity profile of the stimulus, one-quarter carried signals related to linear acceleration (in the form of two peaks of direction selectivity separated in time), and a few neurons followed the derivative of linear acceleration (jerk). In contrast, mainly velocity-coding cells were found in response to rotation. Thus, PIVC comprises a large functional region in macaque areas Ri and S2, with robust responses to 3D rotation and translation, but is unlikely to play a significant role in visual/vestibular integration for self-motion perception.

Representation of vestibular and visual cues to self-motion in ventral intraparietal cortex

Convergence of vestibular and visual motion information is important for self-motion perception. One cortical area that combines vestibular and optic flow signals is the ventral intraparietal area (VIP). We characterized unisensory and multisensory responses of macaque VIP neurons to translations and rotations in three dimensions. Approximately one-half of VIP cells show significant directional selectivity in response to optic flow, one-half show tuning to vestibular stimuli, and one-third show multisensory responses. Visual and vestibular direction preferences of multisensory VIP neurons could be congruent or opposite. When visual and vestibular stimuli were combined, VIP responses could be dominated by either input, unlike the medial superior temporal area (MSTd) where optic flow tuning typically dominates or the visual posterior sylvian area (VPS) where vestibular tuning dominates. Optic flow selectivity in VIP was weaker than in MSTd but stronger than in VPS. In contrast, vestibular tuning for translation was strongest in VPS, intermediate in VIP, and weakest in MSTd. To characterize response dynamics, direction–time data were fit with a spatiotemporal model in which temporal responses were modeled as weighted sums of velocity, acceleration, and position components. Vestibular responses in VIP reflected balanced contributions of velocity and acceleration, whereas visual responses were dominated by velocity. Timing of vestibular responses in VIP was significantly faster than in MSTd, whereas timing of optic flow responses did not differ significantly among areas. These findings suggest that VIP may be proximal to MSTd in terms of vestibular processing but hierarchically similar to MSTd in terms of optic flow processing.

Convergence of Vestibular and Visual Self-Motion Signals in an Area of the Posterior Sylvian Fissure

Convergence of visual motion information (optic flow) and vestibular signals is important for self-motion perception, and such convergence has been observed in the dorsal medial superior temporal (MSTd) and ventral intraparietal areas. In contrast, the parieto-insular vestibular cortex (PIVC), a cortical vestibular area in the sylvian fissure, is not responsive to optic flow. Here, we explore optic flow and vestibular convergence in the visual posterior sylvian area (VPS) of macaque monkeys. This area is located at the posterior end of the sylvian fissure, is strongly interconnected with PIVC, and receives projections from MSTd. We found robust optic flow and vestibular tuning in more than one-third of VPS cells, with all motion directions being represented uniformly. However, visual and vestibular direction preferences for translation were mostly opposite, unlike in area MSTd where roughly equal proportions of neurons have visual/vestibular heading preferences that are congruent or opposite. Overall, optic flow responses in VPS were weaker than those in MSTd, whereas vestibular responses were stronger in VPS than in MSTd. When visual and vestibular stimuli were presented together, VPS responses were dominated by vestibular signals, in contrast to MSTd, where optic flow tuning typically dominates. These findings suggest that VPS is proximal to MSTd in terms of vestibular processing, but distal to MSTd in terms of optic flow processing. Given the preponderance of neurons with opposite visual/vestibular heading preferences in VPS, this area may not play a major role in multisensory heading perception.

Functional Specializations of the Ventral Intraparietal Area for Multisensory Heading Discrimination

The ventral intraparietal area (VIP) of the macaque brain is a multimodal cortical region with directionally selective responses to visual and vestibular stimuli. To explore how these signals contribute to self-motion perception, neural activity in VIP was monitored while macaques performed a fine heading discrimination task based on vestibular, visual, or multisensory cues. For neurons with congruent visual and vestibular heading tuning, discrimination thresholds improved during multisensory stimulation, suggesting that VIP (like the medial superior temporal area; MSTd) may contribute to the improved perceptual discrimination seen during cue combination. Unlike MSTd, however, few VIP neurons showed opposite visual/vestibular tuning over the range of headings relevant to behavior, and those few cells showed reduced sensitivity under cue combination. Our data suggest that the heading tuning of some VIP neurons may be locally remodeled to increase the proportion of cells with congruent tuning over the behaviorally relevant stimulus range. VIP neurons also showed much stronger trial-by-trial correlations with perceptual decisions (choice probabilities; CPs) than MSTd neurons. While this may suggest that VIP neurons are more strongly linked to heading perception, we also find that correlated noise is much stronger among pairs of VIP neurons, with noise correlations averaging 0.14 in VIP as compared with 0.04 in MSTd. Thus, the large CPs in VIP could be a consequence of strong interneuronal correlations. Together, our findings suggest that VIP neurons show specializations that may make them well equipped to play a role in multisensory integration for heading perception.

A Comparison of Vestibular Spatiotemporal Tuning in Macaque Parietoinsular Vestibular Cortex, Ventral Intraparietal Area, and Medial Superior Temporal Area

Vestibular responses have been reported in the parietoinsular vestibular cortex (PIVC), the ventral intraparietal area (VIP), and the dorsal medial superior temporal area (MSTd) of macaques. However, differences between areas remain largely unknown, and it is not clear whether there is a hierarchy in cortical vestibular processing. We examine the spatiotemporal characteristics of macaque vestibular responses to translational motion stimuli using both empirical and model-based analyses. Temporal dynamics of direction selectivity were similar across areas, although there was a gradual shift in the time of peak directional tuning, with responses in MSTd typically being delayed by 100–150 ms relative to responses in PIVC (VIP was intermediate). Responses as a function of both stimulus direction and time were fit with a spatiotemporal model consisting of separable spatial and temporal response profiles. Temporal responses were characterized by a Gaussian function of velocity, a weighted sum of velocity and acceleration, or a weighted sum of velocity, acceleration, and position. Velocity and acceleration components contributed most to response dynamics, with a gradual shift from acceleration dominance in PIVC to velocity dominance in MSTd. The position component contributed little to temporal responses overall, but was substantially larger in MSTd than PIVC or VIP. The overall temporal delay in model fits also increased substantially from PIVC to VIP to MSTd. This gradual transformation of temporal responses suggests a hierarchy in cortical vestibular processing, with PIVC being most proximal to the vestibular periphery and MSTd being most distal.

A robust method for spike sorting with automatic overlap decomposition

Spike sorting is the mandatory first step in analyzing multiunit recording signals for studying information processing mechanisms within the nervous system. Extracellular recordings usually contain overlapped spikes produced by a number of neurons adjacent to the electrode, together with unknown background noise, which in turn induce some difficulties in neural signal identification. In this paper, we propose a robust method to deal with these problems, which employs an automatic overlap decomposition technique based on the relaxation algorithm that requires simple fast Fourier transforms. The performance of the presented system was tested at various signal-to-noise ratio levels based on synthetic data that were generated from real recordings.

Firing rates and dynamic correlated activities of ganglion cells both contribute to retinal information processing.

In the present study, the electrical activities of paired retinal ganglion cells, under full field light stimuli with a variety of chromatic configurations, were recorded from a small functioning piece of retina using multi-electrode array (MEA). Neurons that had increased firings at light-ON and -OFF transients and did not show color-opponent properties were investigated. Single neuronal analysis showed that firing rate of each individual neuron was dependent on the intensity of illumination. Multi-unit analyses revealed that adjacent neurons often fired in synchrony in response to light stimulation. However, in some cases, the strength of correlation between the paired neurons was higher when the retina was exposed to red or green light, and the correlation was attenuated when yellow or white light was given. This seems to suggest that the ensemble activity of non-color-opponent ganglion cells might partly participate in color-information processing, with the red- and green-pathway inputs influencing each other. Such arrangement reflects principle of parsimony: the firing rates of single neuron represent the luminance intensity, and the correlated activities may tell the brain about the color information.

Luminance adaptation increased the contrast sensitivity of retinal ganglion cells.

In the present study, the activity changes of chicken retinal ganglion cells in response to light stimuli with defined contrast were investigated, in the presence of various levels of sustained background illumination. Following a step increase of light illumination, the firing rate of most retinal ganglion cells increased abruptly, and then decreased to a steady-state level with a much lower firing rate during the sustained application of light. However, when a test flash was applied, which superimposed the prolonged background illumination, an increased firing rate was observed. Moreover, the neuron firing rate was increased to a greater extent when the intensity of the background illumination was higher. This may suggest that the neuron sensitivity can be modified by the background illumination level, although the neuron firing rate was reduced during sustained illumination.

Evidence for a Causal Contribution of Macaque Vestibular, But Not Intraparietal, Cortex to Heading Perception

Multisensory convergence of visual and vestibular signals has been observed within a network of cortical areas involved in representing heading. Vestibular-dominant heading tuning has been found in the macaque parietoinsular vestibular cortex (PIVC) and the adjacent visual posterior sylvian (VPS) area, whereas relatively balanced visual/vestibular tuning was encountered in the ventral intraparietal (VIP) area and visual-dominant tuning was found in the dorsal medial superior temporal (MSTd) area. Although the respective functional roles of these areas remain unclear, perceptual deficits in heading discrimination following reversible chemical inactivation of area MSTd area suggested that areas with vestibular-dominant heading tuning also contribute to behavior. To explore the roles of other areas in heading perception, muscimol injections were used to reversibly inactivate either the PIVC or the VIP area bilaterally in macaques. Inactivation of the anterior PIVC increased psychophysical thresholds when heading judgments were based on either optic flow or vestibular cues, although effects were stronger for vestibular stimuli. All behavioral deficits recovered within 36 h. Visual deficits were larger following inactivation of the posterior portion of the PIVC, likely because these injections encroached upon the VPS area, which contains neurons with optic flow tuning (unlike the PIVC). In contrast, VIP inactivation led to no behavioral deficits, despite the fact that VIP neurons show much stronger choice-related activity than MSTd neurons. These results suggest that the VIP area either provides a parallel and partially redundant pathway for this task, or does not participate in heading discrimination. In contrast, the PIVC/VPS area, along with the MSTd area, make causal contributions to heading perception based on either vestibular or visual signals. SIGNIFICANCE STATEMENT Multisensory vestibular and visual signals are found in multiple cortical areas, but their causal contribution to self-motion perception has been previously tested only in the dorsal medial superior temporal (MSTd) area. In these experiments, we show that inactivation of the parietoinsular vestibular cortex (PIVC) also results in causal deficits during heading discrimination for both visual and vestibular cues. In contrast, ventral intraparietal (VIP) area inactivation led to no behavioral deficits, despite the fact that VIP neurons show much stronger choice-related activity than MSTd or PIVC neurons. These results demonstrate that choice-related activity does not always imply a causal role in sensory perception.

Clustering of Self-Motion Selectivity and Visual Response Properties in Macaque Area MSTd

Neurons in the dorsal subdivision of the medial superior temporal area (MSTd) show directionally selective responses to both visual (optic flow) and vestibular stimuli that correspond to translational or rotational movements of the subject. Previous work has shown that MSTd neurons are clustered within the cortex according to their directional preferences for optic flow, suggesting that there may be a topographic mapping of self-motion vectors in MSTd. If MSTd provides a multisensory representation of self-motion information, then MSTd neurons may also be expected to show clustering according to their directional preferences for vestibular signals, but this has not been tested previously. We have examined clustering of vestibular signals by comparing the tuning of isolated single units (SUs) with the undifferentiated multiunit (MU) activity of several neighboring neurons recorded from the same microelectrode. We find that directional preferences for both translational and rotational vestibular stimuli, like those for optic flow, are clustered within area MSTd. MU activity often shows significant tuning for vestibular stimuli, although this MU selectivity is generally weaker for translation than for rotation. When directional tuning is observed in MU activity, the direction preference generally agrees closely with that of a simultaneously recorded SU. We also examined clustering of visual receptive field properties in MSTd by analyzing receptive field maps obtained using a reverse-correlation technique. We find that both the local directional preferences and overall spatial receptive field profiles are well clustered in MSTd. Overall, our findings have implications for how visual and vestibular signals regarding self-motion may be decoded from populations of MSTd neurons.