Discrimination between active and passive head movements by macaque ventral and medial intraparietal cortex neurons

Abstract

An important prerequisite for effective motor action is the discrimination between active and passive body movements. Passive movements often require immediate reflexes, whereas active movements may demand suppression of the latter. The vestibular system maintains correct body and head posture in space through reflexes. Since vestibular inputs have been reported to be largely suppressed in the vestibular nuclei during active head movements, we investigated whether head movement-related signals in the primate parietal cortex, a brain region involved in self-motion perception, could support both reflex functions and self-movement behaviour. We employed a paradigm that made available direct comparison of neuronal discharge under active and passive movement conditions. In this study, we demonstrate that a population of intraparietal (VIP (ventral) and MIP (medial)) cortex neurons change their preferred directions during horizontal head rotations depending on whether animals have performed active movements, or if they were moved passively. In other neurons no such change occurred. A combination of these signals would provide differential information about the active or passive nature of an ongoing movement. Moreover, some neurons' responses clearly anticipated the upcoming active head movement, providing a possible basis for vestibular-related reflex suppression. Intraparietal vestibular neurons thus distinguish between active and passive head movements, and their responses differ substantially from those reported in brainstem vestibular neurons, regarding strength, timing, and direction selectivity. We suggest that the contextual firing characteristics of these neurons have far-reaching implications for the suppression of reflex movements during active movement, and for the representation of space during self-movement.

Figure 1. Recording sites and active–passive replay paradigm

A, location and reconstruction of recording sites. Overall lateral view of the left hemisphere of a macaque monkey indicating the main cortical landmarks: intraparietal sulcus, ips; central sulcus, cs; lateral fissure, lf. The broken line indicates the placement of the coronal section shown below, with reconstructed typical electrode tracks and recording sites (MIP, medial intraparietal area; VIP, ventral intraparietal area) in the intraparietal sulcus. Area VIP is highlighted in light grey, and area MIP in dark grey. (LIP, lateral intraparietal area; sts, superior temporal sulcus). B, the animal was allowed spontaneous horizontal head movements in darkness while neuronal discharges and head movement trajectories were recorded. C, subsequently, the animal's head was fixed, and the previously recorded head movement was replayed with a horizontal turntable, again monitoring neuronal firing.

Figure 2. Comparison of neuronal firing characteristics during active and passive head movements: quantitative differences (firing intensity differences)

Left-hand columns (Aa, Ba, Ca) show firing behaviour (Rate) during active and passive (replay) horizontal head movements (H Head). Head movement trajectories are depicted as position traces (black lines), and as velocity profiles (red shading). Upward deflections symbolize movement to the right, and vice versa. Velocity traces were divided by a factor of 10 for graphical scaling purposes. Right-hand columns (Ab, Bb, Cb) depict mean firing rates as a function of head velocity for the same neurons. Small vertical bars represent standard error. Vertical dotted lines indicate change-over points between leftward (negative) and rightward (positive) velocities. Aa, Type II neuron only active during passive rotation. Ab, the velocity traces emphasize that this neuron does not respond during active movement, but that it shows a clear preference for rightward head movements (i.e. positive velocities) under passive conditions (Type II). Ba, Type II neuron only active during active head movement. Bb, velocity traces indicate that the neuron responds during rightward active head movements (Type II), but is silent during passive head rotation. Ca, Type III neuron whose activity is greater during passive stimulation. Cb, velocity traces show that the neuron responds to head movements in both directions (Type III) under active as well as passive movement conditions, but its response intensity is much greater in the passive condition.

Figure 3. Comparison of neuronal firing characteristics during active and passive head movements: qualitative differences (preferred direction and timing differences)

Left-hand columns (Aa, Ba, Ca) show firing behaviour (Rate) during active and passive (replay) horizontal head movements (H Head). Head movement trajectories are depicted as position traces (black lines), and as velocity profiles (red shading). Upward deflections symbolize movement to the right, and vice versa. Velocity traces were divided by a factor of 10 for graphical scaling purposes. Vertical dotted lines in Ba and Ca indicate the sampling periods used for quantitative data analysis. Right-hand columns (Ab, Bb, Cb) depict mean firing rates as a function of head velocity for the same neurons. Small vertical bars represent standard error. Vertical dotted lines indicate change-over points between leftward (negative) and rightward (positive) velocities. Aa, change of directional selectivity: under active movement conditions, the neuron shows Type II behaviour, under passive stimulation Type I behaviour. In addition, neuronal activity is greater during passive head movements, than during active stimulation. Ab, velocity traces clearly show the change of preferred direction: the neuron shows a Type II behaviour (increase of firing towards positive velocity or rotation to the right) during active head movement, and Type I behaviour (increase of firing towards negative velocity or rotation to the left) during passive stimulation. Ba, change of directional selectivity: this neuron shows Type I behaviour during active head movements (responding clearly more strongly to leftward then to rightward head velocities), and a Type III response following passive rotation. In this case, response strength remains about the same. Bb, velocity traces show Type I behaviour (dominant increase of firing towards negative velocity or rotation to the left) during active head movement, and change to a Type III response (equivalent increase of firing towards negative and positive velocities) during passive stimulation. Ca, anticipatory response to active movement: Type II neuron with a response build-up starting before the active movement; response to passive movement, naturally, begins with rotation onset. Cb, velocity traces show that the neuron responds to rightward velocities (Type II) during active and passive movements, but the response is greater in the passive condition.

Figure 4. Quantitative comparison of response strengths of intraparietal neurons between active and passive movement conditions

Mean percentages of observations, i.e. (P₁ + P₂)/2 are given for the three classes, with grey shading indicating the relative distribution of these values for the two animals. Error bars indicate the 95% confidence intervals of the percentages. Most cells had a weaker response to active movement (51/67 and 16/18 for monkeys 1 and 2, respectively, i.e. 79% of the total population). However, a small but sizeable proportion of neurons responded with equal strength under both movement conditions (8/67 and 0/18 for monkeys 1 and 2, respectively, i.e. 9%) or more vigorously to active movements (8/67 and 2/18 for monkeys 1 and 2, respectively, i.e. 12%).

Figure 5. Response latencies of firing rates relative to the onset of head movements

A, distribution for active movements. B, passive movement condition. Mean percentages of observations, i.e. (P₁ + P₂)/2 are given for each class with grey shading indicating the relative distribution of values for the two animals. Bin width was set to 100 ms. Under both conditions, most neurons started firing within 150 ms after the beginning of head movements (102/108 and 80/86 for active and passive movements, respectively). For active movements, a fair number of cells started firing at least 50 ms before the onset of head movements (21/108), and one cell had already fired about 350 ms before the movement.

Figure 6. Effect of neck input on parietal vestibular neurons

A, Passive sinusoidal rotation (whole-body rotation, WBR). B, trunk-under-head rotation (passive neck rotation, PNR). The two top rows show neuronal firing rates as histograms (bin width 100 ms) and as raster plots, the two bottom rows show relative neck rotation (PNR) and whole-passive-body rotation (WBR). The vertical broken line indicates the change from rightward (up) to leftward (down) rotation. In this case of a Type II neuron, 10 rotations were superimposed/averaged. In A, only passive sinusoidal rotation was used with the animal's head fixed to the turntable, i.e. head and body were rotated together (classical paradigm), and no PNR occurred as symbolized by the straight line. In B, the animal's head was held fixed in space, while its body was rotated passively underneath. The bottom two rows indicate the direction of trunk rotation (WBR) and the direction of relative head rotation with respect to the trunk (PNR), although in this case, no vestibular stimulation occurred. Equivalent relative neuronal firing rates are indicated by grey shading. In such cases, vestibular and neck inputs would work synergistically, although the neck component is considerably smaller than the vestibular contribution.

Figure 7. Discrimination between active and passive movements by intraparietal neurons, depending on selectivity to movement type (active A: blue; passive P: magenta) and direction (left or right: arrows)

In the illustrated examples, discrimination between an active (A) and a passive head rotation (B) to the left is elaborated. In the general scheme, a set of input neurons (IN1–IN4) is connected in a particular fashion to a set of output neurons (OUT1–OUT4). With regard to the preferred directions of vestibular responses, two types of input neuron populations are distinguished when comparing active and passive movement, i.e. neurons which change their preferred direction depending on active or passive mode (IN1, IN3), and those that do not (IN2, IN4). In case of discriminating an active head movement to the left (A), two neurons would be involved, the first (IN1) responding with activation during leftward active movement and rightward passive movement, and another (IN2) responding to both leftward active and passive movements. An output neuron (OUT1) receiving afferents (bold lines) from these two neurons, would signal only leftward active movements. In such case, the two components signalling leftward active movement would get reinforced, whereas the components signalling leftward and rightward passive movement would oppose each other and cancel out (neurons not involved are shaded in grey). In the case of a passive movement (B), a population of output neurons (OUT2) receiving afferents from neurons activated during active and passive leftward movement (IN2), and from those responding to leftward passive and rightward active movements (IN3), would signal leftward passive movement. In this case, the two components signalling leftward and rightward active movement would oppose each other and cancel out, whereas the two leftward passive movement-signalling components would reinforce each other (again, neurons not involved are shaded in grey). The two other distinct types for active and passive rightward movements (OUT3, OUT4) are constructed analogously.