Neural coding and perceptual detection in the primate somatosensory thalamus

Abstract

The contribution of the sensory thalamus to perception and decision making is not well understood. We addressed this problem by recording single neurons in the ventral posterior lateral (VPL) nucleus of the somatosensory thalamus while trained monkeys judged the presence or absence of a vibrotactile stimulus of variable amplitude applied to the skin of a fingertip. We found that neurons in the VPL nucleus modulated their firing rate as a function of stimulus amplitude, and that such modulations accounted for the monkeys' overall psychophysical performance. These neural responses did not predict the animals' decision reports in individual trials, however. Moreover, the sensitivity to changes in stimulus amplitude was similar when the monkeys' performed the detection task and when they were not required to report stimulus detection. These results suggest that the primate somatosensory thalamus likely provides a reliable neural representation of the sensory input to the cerebral cortex, where sensory information is transformed and combined with other cognitive components associated with behavioral performance.

Fig. 1.

Detection task, psychophysical performance, and recording area. (A) Trials began when the stimulator probe indented the skin of one fingertip of the monkey’s restrained right hand (PD). Then the monkey placed its free, left hand on an immovable key (KD, key down). After a variable prestimulus period (1.5–3 s), in one-half of the trials a vibratory stimulus of 20 Hz (variable amplitude, 1–34 μm) was delivered to the glabrous skin of one fingertip. In the other half of the trials, no stimulus was delivered. Ten repetitions per stimulus amplitude were presented, counterbalanced with the same number of stimulus-absent trials, all interleaved at random. After stimulus presentation, the monkey waited for 2 or 3 s until the probe was lifted (PU). This was the cue signal to remove its free hand from the key (KU, key up) and indicate whether the stimulus was present or absent by pressing one of two response buttons. The time interval between KU and button press (PB) is shown in all figures as movement time (MT). (B) The detection task elicited four behavioral responses: hits or misses during stimulus-present trials and CRs or FAs during stimulus-absent trials. (C) Psychometric function showing the probability that the monkey reports the presence of the stimulus, as a function of stimulus amplitude. Each point represents an average over 58 sessions. The line is a Boltzmann fit to the data points. Its amplitude modulation (ΔA = 0.87) is the difference in probability between the maximum and minimum amplitudes. The detection threshold (t_p = 8.0 μm) and slope of the curve (s_p = 0.062 μm⁻¹) at a probability of 0.5 are indicated. (D) The recording site at the VPL nucleus of the somatosensory thalamus.

Fig. 2.

Activity of two VPL neurons during the detection task. (A) Raster plot of a QA neuron. Each row is a trial, and each black tick represents the time at which an action potential occurred. Trials are arranged according to stimulus amplitude, shown on the left. Blue and red marks indicate behavioral responses: hits and misses, respectively, for stimulus-present trials and CRs and FAs, respectively, for stimulus-absent trials. The upper line indicates relevant task events (PD and PU) and the monkey’s MT. The gray box depicts the stimulation period. (B) Firing rate (blue) and power at 20 Hz (green) as functions of stimulus amplitude (mean ± SD; n = 10 trials). The blue and green lines correspond to linear regression fits. The slopes for each fit are indicated. Slopes were significantly different from 0 exclusively during the stimulation period (P ≤ 0.05). (C) Raster plot of an SA neuron, with the same conventions as in B. (D) Slopes were significantly different from 0 during the stimulus period.

Fig. 3.

Comparison of VPL activity and psychophysical performance during the detection task. All plots show the probability that the monkey's or the neuron's response indicated that a stimulus was present (“yes”) as a function of stimulus amplitude. (A, C, and E) Individual psychometric and neurometric curves. The black lines indicate the monkey’s probability of detection during each recording session. The red lines indicate each neuron’s probability of detection based on either the firing rate (A and E) or periodicity (C) exceeding a criterion threshold. In A and C, firing rate and periodicity were computed over a 500-ms window during the stimulation period. In E, firing rate was computed over a 50-ms window during the stimulation period. (B, D, and F) Mean psychometric (black) and neurometric (red) curves, obtained by averaging the corresponding groups of curves in A (n = 51), C (n = 58), and E (n = 30). ∆A_p and s_p (∆A_n and s_n) indicate the amplitude modulation and slope of the average psychometric (neurometric) curves, respectively.

Fig. 4.

Population response of VPL neurons to a sinusoidal stimulus. In all panels, 0 indicates stimulus onset. (A) Representation of a periodic sinusoidal wave with an amplitude of 34 μm applied to the skin of a fingertip. (B) Mean spike density function (SDF) for the population of VPL neurons (n = 54) in response to the stimulus shown in A. The SDF indicates the presence of more spikes within the first pulses of the stimulus compared with the last pulses. The SDF was calculated using a 2-ms-wide Gaussian filter. (C) Slopes (mean ± SD; n = 63) calculated at different times after onset of stimulus. Slopes indicate neuronal sensitivity to changes in stimulus amplitude, calculated by fitting a linear regression to the firing rate as a function of the stimulus amplitude (0–34 μm). Firing rates were calculated within a 50-ms window at different times after the onset of stimulus. Only significant slopes were used in the analysis. The sensitivity to changes in stimulus amplitude was significantly lower after the fourth sinusoidal pulse compared with the first sinusoidal wave (*P = 0.001).

Fig. 5.

Correlation between VPL activity and the monkeys’ perceptual judgments. (A) Comparison of normalized neuronal responses for hits (n = 372, black line) and misses (n = 376, red line) during near-threshold stimulation (Left) and for CRs (n = 873, black line) and FAs (n = 873, red line) during stimulus-absent trials (Right). Upper lines and gray boxes indicate relevant task events (stimulus onset and offset, PU, and MT). (B) Choice probability as a function of time. The black solid line represents the choice probability index between hits and misses for near-threshold trials (Left) and between FAs and CRs for stimulus-absent trials (Right). The dashed gray lines represent mean choice probability values obtained by resampling the values from the original distributions 1,200 times, thereby shuffling the hit/miss and the CR/FA labels. Mean choice probability values were 0.4766 ± 0.14 for the stimulus-present trials and 0.5 ± 0.0004 for the stimulus-absent trials. No significant values were found (α = 0.01).

Fig. 6.

Responses of VPL neurons during task performance versus passive stimulation. Slopes were obtained from the linear regression fits performed on the firing rate as a function of stimulus amplitude for 28 neurons recorded in two conditions: during active detection and during passive delivery of the stimuli, for which no responses by the monkeys were required. Points are close to the diagonal, indicating similar slopes in the two conditions. No significant differences were found (P = 0.56; n = number of neurons). The red cross indicates the slope values for active detection (mean ± SEM, 1.22 ± 0.16 Hz/μm) and passive stimulation (1.08 ± 0.14 Hz/μm).