Gravity orientation tuning in macaque anterior thalamus

Abstract

Gravity may provide a ubiquitous allocentric reference to the brain's spatial orientation circuits. Here we describe neurons in the macaque anterior thalamus tuned to pitch and roll orientation relative to gravity, independently of visual landmarks. We show that individual cells exhibit two-dimensional tuning curves, with peak firing rates at a preferred vertical orientation. These results identify a thalamic pathway for gravity cues to influence perception, action and spatial cognition.

Figure 1. Neuronal responses during yaw rotations around upright and tilted axes

(a–d) Example neuron responses during (a) yaw rotation around an earth-vertical axis, with the animal upright (in light), yaw rotations around axes tilted ±30° in light (b,c) and darkness (d). Abbreviations: NU: nose-up, ND: nose down, LED: left ear down, RED: right ear down. Upper row: illustration of the stimuli. Middle row: neuronal responses as a function of head orientation relative to the visual environment (a–d, top axis) or relative to gravity (b–d, lower axis). The drawings below the plots illustrate head position in space. Red/Blue raster plots and lines: individual spikes and average response during multiple cycles of counterclockwise (CCW) and clockwise (CW) rotation respectively. Neuron recorded in Animal L, right hemisphere. A total of 48 neurons were recorded. (e–h) Population responses (n=48). (e,g) Resultant (R) vector length. (e) Comparison between +30° and −30° tilt. (g) Comparison between rotations in light and darkness. (f,h) Distributions of the absolute difference in Preferred Direction (PD) relative to gravity between (f) +30° and −30° tilt, and (h) rotations in light and darkness. Each cell appears twice in red/blue plots (for CCW and CW rotations, respectively).

Figure 2. Gravity (G) and Gravity-derivative (velocity, dG) responses

Cells are classified as G-tuned (green), dG-tuned (cyan) and G+dG-tuned (gray) (see Suppl. Fig. 6 for details). (a,b) Comparison of resultant vector length, |R|, and PD between CW and CCW rotations. Cells showed similar modulation strength during CW (|R| = 0.36 ± 0.2 SD) and CCW (|R| = 0.35± 0.2 SD) rotation (paired Wilcoxon rank test, p=0.93), but often differed in PD. Identical PDs are characteristic of G-tuned whereas opposite PDs are characteristic of dG-tuned cells. (c) Resultant vector length, |R|, of the G and dG components. G-tuned cells: |R(G)| = 0.37 ± 0.2 SD, |R(dG)| = 0.11 ± 0.1 SD; dG-tuned cells: |R(G)| = 0.18 ± 0.1 SD, |R(dG)| = 0.33 ± 0.1 SD. (d) Distribution of the preferred direction of the G component (upper panel, G-tuned and G+dG-tuned cells) and dG component (lower panel, dG-tuned and G+dG-tuned cells). ND, Contralateral (Cont.), NU and Ipsilateral (Ipsi.) refer to the direction of tilt (G component) or tilt velocity (dG component).

Figure 3. Example cell exhibiting hill-shaped tuning to Gravity and population summary

(a) Responses during rotation in upright orientation ±5° to ±45° tilt (positive and negative tilt are averaged). 31 cells were recorded with this protocol. (b) Two-dimensional gravity (G) tuning curve of this example cell, extracted from the data. In this polar plot, the distance from the center represents the tilt angle and the 360° circular angle represents the direction of the tilt (Suppl. Fig. 1d). Note that, because of the elongated shape of the hill of activity, the cell fires at 5–10 spk/s in LED and RED at 45° tilt, and is silent in NU and ND, leading to the double-peaked response during yaw rotation with ±45° tilt. (c) Location of the peak response for G-tuned cells (n=18) and dG-tuned cells (n=5). ND, Contralateral, NU and Ipsilateral refer to the direction of tilt for G-tuned cells and the direction of tilt velocity for dG-tuned cells. (d) Cumulative distribution of preferred tilt angles for G-tuned cells (n=13). Black curve: expected cumulative distribution assuming that the cells are distributed uniformly. Cells with preferred angle > 40° (n=5) are excluded from the cumulative distribution.