Response dynamics and tilt versus translation discrimination in parietoinsular vestibular cortex

Abstract

The parietoinsular vestibular cortex (PIVC) is a large area in the lateral sulcus with neurons that respond to vestibular stimulation. Here we compare the properties of PIVC cells with those of neurons in brain stem, cerebellum, and thalamus. Most PIVC cells modulated during both translational and rotational head motion. Translation acceleration gains showed a modest decrease as stimulus frequency increased, with a steeper slope than that reported previously for thalamic and cerebellar nuclei neurons. Response dynamics during yaw rotation were similar to those reported for vestibular neurons in brain stem and thalamus: velocity gains were relatively flat through the mid-frequency range, increased at high frequencies, and decreased at low frequencies. Tilt dynamics were more variable: PIVC neurons responsive only to rotation had gains that decreased with increased frequency, whereas neurons responsive during both translation and rotation (convergent neurons) actually increased their modulation magnitude at high frequencies. Using combinations of translation and tilt, most PIVC neurons were better correlated with translational motion; only 14% were better correlated with net acceleration. Thus, although yaw rotation responses in PIVC appear little processed compared with other central vestibular neurons, translation and tilt responses suggest a further processing of linear acceleration signals in thalamocortical circuits.

Figure 1.

Magnetic resonance imaging–based reconstruction of recording locations. (A, C) Flat maps of the brain areas (color coded) around the lateral sulcus of the right hemisphere of monkey U (A) and the right hemisphere of monkey J (C), with cell locations mapped onto the surface. (B, D) Corresponding coronal sections with the 3 major sulci (IPS, LS, and STS) identified. Each dot corresponds to a cell responsive to vestibular stimulation (n = 93), color coded as follows: convergent (n = 62, yellow), translation only (17, blue), and rotation only (n = 14, pink). 7op, area 7 operculum; Ig, granular insula; IPS, intraparietal sulcus; LS, lateral sulcus; Ri, retroinsular area; S2, secondary somatosensory area; STS, superior temporal sulcus.

Figure 2.

Example PIVC neuron responses during (A) yaw rotation, (B) pitch rotation, (C) roll rotation, (D) lateral translation, and (E) fore–aft translation (0.5 Hz). IFR, instantaneous firing rate; Stim, head angular velocity (A, B, C) or linear acceleration (D and E); sp, spikes; G = 9.8 m/s².

Figure 3.

Distributions of preferred direction, gain, and phase. (A) Polar plot of maximum response direction and gain during translation (0.5 Hz). Each data point corresponds to a cell (n = 79). The distance of each data point from the center corresponds to the neuron's response gain (in units of spikes per second per G, G = 9.81 m/s²), whereas its polar angle illustrates the cell's preferred direction in the horizontal plane (see cartoon). Filled circles: convergent neurons (n = 62); open circles: nonconvergent neurons (n = 17). (B) Distribution of response phase (computed for the preferred direction). A phase of 0° illustrates responses in phase with acceleration. (C) Distribution of tuning ratio, computed as the ratio of the gains along the preferred and orthogonal response directions. Filled versus open bars illustrate convergent (i.e., responding to both rotation and translation) and nonconvergent (i.e., sensitive only to translation) neurons, respectively.

Figure 4.

Example PIVC neuron responses during combinations of tilt and translation. (A) Translation only, (B) tilt only, (C) tilt − translation, and (D) tilt + translation (0.5 Hz). Data are shown along 2 stimulation axes (cartoon drawings), with the translation/tilt position (bottom traces) being matched in both amplitude and direction to elicit an identical net acceleration in the horizontal plane. Vertical dotted lines mark the times of peak stimulus amplitude.

Figure 5.

Summary of tilt/translation responses. Peak response amplitude and phase during (A, D) tilt, (B, E) tilt − translation, and (C, F) tilt + translation are plotted as a function of the corresponding response during translation (0.5 Hz, n = 71). Filled symbols: convergent neurons; open symbols: nonconvergent neurons. Solid red lines indicate the predictions when cells selectively encode translation, whereas dashed blue lines illustrate the predictions of encoding net linear acceleration.

Figure 6.

Summary of tilt/translation responses. Scatter plot of z-transformed partial correlation coefficients for fits of each cell responses with translation and net acceleration-coding models (n = 71). The superimposed dashed lines divide the plot into 3 regions: an upper/left area corresponding to cell responses that were significantly better fit (P < 0.01) by the translation-coding model; a lower/right area that includes neurons that were significantly better fit by the net acceleration model; and an in-between area that would include cells that were not significantly better fit by either model. Filled symbols: convergent neurons; open symbols: nonconvergent neurons.

Figure 7.

Summary of PIVC cell dynamics during translation. (A) Instantaneous firing rate (IFR) of an example PIVC cell during lateral and fore–aft translation at 0.161, 0.5, and 2 Hz. (B, C) Response gain and phase (expressed relative to linear acceleration and computed along the preferred direction) of each PIVC cell (n = 26; gray symbols and lines) are plotted versus frequency. Black thick lines and symbols illustrate the population averages. (D, E) Mean normalized gain and phase (±standard deviation) of PIVC neurons (black) are compared with the corresponding data from MSTd (red; replotted with permission from Liu and Angelaki 2009), thalamus (dark yellow; replotted with permission from Meng et al. 2007), CN (blue; replotted with permission from Shaikh, Ghasia, et al. 2005), and simple spikes of nodulus/uvula Purkinje cells (cyan; replotted with permission from Yakusheva et al. 2008).

Figure 8.

Summary of PIVC cell dynamics during yaw rotation. (A) Instantaneous firing rate (IFR) of an example PIVC cell during yaw rotation at 0.05, 0.1, 0.5, and 2 Hz. (B, C) Response gain and phase (expressed relative to angular velocity) of each PIVC cell (n = 11; gray symbols and lines) are plotted versus frequency. Black thick lines/symbols illustrate population averages. (D, E) Mean normalized gain and phase (±standard deviation) of PIVC neurons (black) are compared with the corresponding data from the VN (green; replotted with permission from Dickman and Angelaki 2004) and thalamus (dark yellow; replotted with permission from Meng et al. 2007). Data from regular and irregular canal afferents are also shown for comparison (red dashed and dotted lines; replotted with permission from Haque et al. 2004).

Figure 9.

Summary of PIVC cell dynamics during tilt. (A) Instantaneous firing rate (IFR) of 2 example PIVC cells during tilt at 0.05, 0.1, 0.5, and 2 Hz. (B, C) Response gain and phase (expressed relative to angular velocity) of each PIVC cell (n = 16; gray: convergent cells; black: nonconvergent cells) are plotted versus frequency. (D, E) Mean normalized gain and phase (±standard deviation) of PIVC neurons (black) are compared with corresponding data from the VN (green; replotted with permission from Dickman and Angelaki 2004) and simple spikes of nodulus/uvula Purkinje cells (cyan; replotted with permission from Yakusheva et al. 2008).