Probing the cortical neuronal correlates of a sensory discrimination process.

Key to understanding perception is the form of how sensory stimuli are represented in the evoked activity of the brain. Here, we addressed the question of which components of the evoked neuronal activity in the somatosensory cortex represent the stimulus features while trained monkeys discriminated the difference in frequency between two vibrotactile stimuli. We probed whether these cortical neuronal representations are essential to perception. The results show a strong link between the cortical representation of the stimulus and perception.

[Neural codes for perception]. / Códigos neurales para la percepción.

OBJECTIVE: This article describes experiments designed to show the neural codes associated with the perception and processing of tactile information. DEVELOPMENT: The results of these experiments have shown the neural activity correlated with tactile perception. The neurones of the primary somatosensory cortex (S1) represent the physical attributes of tactile perception. We found that these representations correlated with tactile perception. By means of intracortical microstimulation we demonstrated the causal relationship between S1 activity and tactile perception. In the motor areas of the frontal lobe is to be found the connection between sensorial and motor representation whilst decisions are being taken. CONCLUSIONS: S1 generates neural representations of the somatosensory stimuli which seen to be sufficient for tactile perception. These neural representations are subsequently processed by central areas to S1 and seem useful in perception, memory and decision making.

Códigos neurales para la percepción / Neural codes for perception

Objetivo. Este artículo describe experimentos diseñados para poner en evidencia los códigos neurales asociados a la percepción y el procesamiento de información táctil. Desarrollo. Los resultados obtenidos en estos experimentos han revelado la actividad neural correlacionada con la percepción táctil. Las neuronas de la corteza somatosensorial primaria (S1) representan los atributos físicos de los estímulos táctiles. Se encontró que estas representaciones se correlacionan con la percepción táctil. Se comprobó por medio de la microestimulación intracortical la relación causal entre la actividad de S1 y la percepción táctil. En las áreas motoras del lóbulo frontal se encontró el enlace entre las representaciones sensoriales y motoras durante la toma de decisiones. Conclusiones. S1 genera representaciones neurales de los estímulos somatosensoriales que parecen ser suficientes para la percepción táctil. Estas representaciones neurales son posteriormente procesadas por áreas centrales a S1 y parecen ser útiles para la percepción, memoria y la toma de decisiones (AU)

Periodicity and firing rate as candidate neural codes for the frequency of vibrotactile stimuli.

The flutter sensation is felt when mechanical vibrations between 5 and 50 Hz are applied to the skin. Neurons with rapidly adapting properties in the somatosensory system of primates are driven very effectively by periodic flutter stimuli; their evoked spike trains typically have a periodic structure with highly regular time differences between spikes. A long-standing conjecture is that, such periodic structure may underlie a subject's capacity to discriminate the frequencies of periodic vibrotactile stimuli and that, in primary somatosensory areas, stimulus frequency is encoded by the regular time intervals between evoked spikes, not by the mean rate at which these are fired. We examined this hypothesis by analyzing extracellular recordings from primary (S1) and secondary (S2) somatosensory cortices of awake monkeys performing a frequency discrimination task. We quantified stimulus-driven modulations in firing rate and in spike train periodicity, seeking to determine their relevance for frequency discrimination. We found that periodicity was extremely high in S1 but almost absent in S2. We also found that periodicity was enhanced when the stimuli were relevant for behavior. However, periodicity did not covary with psychophysical performance in single trials. On the other hand, rate modulations were similar in both areas, and with periodic and aperiodic stimuli, they were enhanced when stimuli were important for behavior, and were significantly correlated with psychophysical performance in single trials. Thus, the exquisitely timed, stimulus-driven spikes of primary somatosensory neurons may or may not contribute to the neural code for flutter frequency, but firing rate seems to be an important component of it.

Sensing without touching: psychophysical performance based on cortical microstimulation.

Unequivocal proof that the activity of a localized cortical neuronal population provides sufficient basis for a specific cognitive function has rarely been obtained. We looked for such proof in monkeys trained to discriminate between two mechanical flutter stimuli applied sequentially to the fingertips. Microelectrodes were inserted into clusters of quickly adapting (QA) neurons of the primary somatosensory cortex (S1), and the first or both stimuli were then substituted with trains of current pulses during the discrimination task. Psychophysical performance with artificial stimulus frequencies was almost identical to that measured with the natural stimulus frequencies. Our results indicate that microstimulation can be used to elicit a memorizable and discriminable analog range of percepts, and shows that activation of the QA circuit of S1 is sufficient to initiate all subsequent neural processes associated with flutter discrimination.

Neuronal correlates of sensory discrimination in the somatosensory cortex.

Monkeys are able to discriminate the difference in frequency between two periodic mechanical vibrations applied sequentially to the fingertips. It has been proposed that this ability is mediated by the periodicity of the responses in the quickly adapting (QA) neurons of the primary somatosensory cortex (S1), instead of the average firing rates. We recorded from QA neurons of S1 while monkeys performed the vibrotactile discrimination task. We found that the periodic mechanical vibrations can be represented both in the periodicity and in the firing rate responses to varying degrees across the QA neuronal population. We then computed neurometric functions by using both the periodicity and the firing rate and sought to determine which of these two measures is associated with the psychophysical performance. We found that neurometric thresholds based on the firing rate are very similar to the animal's psychometric thresholds whereas neurometric thresholds based on periodicity are far lower than those thresholds. These results indicate that an observer could solve this task with a precision similar to that of the monkey, based only on the firing rate produced during the stimulus periods.

Somatosensory discrimination based on cortical microstimulation.

The sensation of flutter is produced when mechanical vibrations in the range of 5-50Hz are applied to the skin. A flutter stimulus activates neurons in the primary somatosensory cortex (S1) that somatotopically map to the site of stimulation. A subset of these neurons-those with quickly adapting properties, associated with Meissner's corpuscles-are strongly entrained by periodic flutter vibrations, firing with a probability that oscillates at the input frequency. Hence, quickly adapting neurons provide a dynamic representation of such flutter stimuli. However, are these neurons directly involved in the perception of flutter? Here we investigate this in monkeys trained to discriminate the difference in frequency between two flutter stimuli delivered sequentially on the fingertips. Microelectrodes were inserted into area 3b of S1 and the second stimulus was substituted with a train of injected current pulses. Animals reliably indicated whether the frequency of the second (electrical) signal was higher or lower than that of the first (mechanical) signal, even though both frequencies changed from trial to trial. Almost identical results were obtained with periodic and aperiodic stimuli of equal average frequencies. Thus, the quickly adapting neurons in area 3b activate the circuit leading to the perception of flutter. Furthermore, as far as can be psychophysically quantified during discrimination, the neural code underlying the sensation of flutter can be finely manipulated, to the extent that the behavioural responses produced by natural and artificial stimuli are indistinguishable.

Categorical perception of somesthetic stimuli: psychophysical measurements correlated with neuronal events in primate medial premotor cortex.

In this paper we describe a type of neuron of the medial premotor cortex (MPC) that discharged differentially during a categorization task and reflected in their activity whether the speed of a tactile stimulus was low or high. The activity of these neurons was recorded in the MPC contralateral (right MPC, n = 88) and ipsilateral (left MPC, n = 103) to the stimulated hand of four monkeys performing this somesthetic task. Animals performed the task by pressing with the right hand one of two target switches to indicate whether the speed of probe movement across the skin of the left hand was low or high. Differential responses of MPC neurons occurred during the stimulus and reaction time period. We used an analysis based on signal detection theory to determine whether these differential responses were associated with the animal's decision. According to this analysis, 104 of the 191 neurons (right MPC, n = 48; left MPC, n = 56) coded the categorization of the stimulus speeds (categorical neurons). In a light instruction task, we tested the possibility that the categorical neurons (n = 71) were associated with the intention to press, or with the trajectory of the hand to one of the two target switches used to indicate categorization. In this situation, each trial began as in the somesthetic categorization task, but one of the two target switches was illuminated beginning with the skin indentation, continued during the delay period and turned off when the probe was lifted off from the skin. This condition instructed the animal which target switch was required to be pressed for reward. Very few neurons (14 of 71) maintained their differential responses observed in the categorization task. Some categorical neurons (n = 5) were also studied; the animal categorized the tactile stimulus speeds, but knew in advance whether the stimulus speed was low or high (categorization + light instruction). This was made by illuminating one of the two target switches which was associated with the stimulus speed. The categorical response was considerably attenuated in this condition. Interestingly, during the delay period, these neurons reflected in their activity whether the stimulus was low or high. A number of the categorical MPC neurons (n = 30) were studied when the same set of stimuli, used in the categorization, were delivered passively. None of these neurons responded in this condition. These results suggest that the MPC, apart from its well-known role in motor behavior, is also involved in the animal's decision during the execution of this learned somesthetic task.

Role of primary somatic sensory cortex in the categorization of tactile stimuli: effects of lesions.

We lesioned the right primary somatic sensory (S1) cortex in two monkeys trained to categorize the speed of moving tactile stimuli. Animals performed the task by pressing with the right hand one of two target switches to indicate whether the speed of a probe moving across the glabrous skin of the left hand was low or high. Sensory performance was evaluated with psychometric techniques and motor behavior was monitored by measuring the reaction (RT) and movement (MT) times before the experiment and throughout the 60 days after the ablation of SI cortex. After the lesion, there was a slight increase in the RTs but no change in the MTs, indicating that removal of SI cortex did not affect the animals' capacity to detect the stimuli. However, monkeys lost their ability to categorize the stimulus speeds. This effect was observed from the 1st day after the lesion until the end of the study. We conclude that somatosensory areas outside SI can by themselves process tactile information in a limited way and that the extraction of higher-order features that takes place during the categorization task requires the intervention of SI cortex.

Functional properties of primate putamen neurons during the categorization of tactile stimuli.

We used psychometric techniques and neurophysiological recordings to study the role of the putamen in somesthetic perception. Four monkeys were trained to categorize the speed of moving tactile stimuli. Animals performed a task in which one of two target switches had to be pressed with the right hand to indicate whether the speed of probe movement across the glabrous skin of the left, restrained hand was low or high. During the task we recorded the activity of neurons in the putamen contralateral (right) and ipsilateral (left) to the stimulated hand. We found different types of neuronal responses, all present in the right and left putamen. Some neurons responded during the stimulus period, others responded during the hand-arm movement used to indicate categorization, and others responded during both of these periods. The responses of many neurons did not vary either with the speed of the stimuli or in relation to the categorization process. In contrast, neurons of a particular type responded differentially: their activity reflected whether stimulus speed was low or high. These differential responses occurred during the stimulus and hand-arm motion periods. A number of the nondifferential and differential neurons were studied when the same stimuli used in the categorization task were delivered passively. Few neurons with nondifferential discharges, and none of the differential neurons, responded in this condition. In a visually cued control task we studied the possibility that the differential responses were associated with the intention to press or with the trajectory of the hand to one of the target switches. In this condition, a light turned on instructed the animal which target switch to press for a reward. Very few neurons in both hemispheres maintained the differential responses observed during the categorization task. Those neurons that discharged selectively for low or high speeds were analyzed quantitatively to produce a measure comparable with the psychometric function. The thresholds of the resulting neurometric curves for the neuronal populations were very similar to the psychometric thresholds. The activity of a large fraction of these neurons could be used to accurately predict whether the stimulus speed was low or high. The results indicate that the putamen, both contralateral and ipsilateral to the stimulated hand, contains neurons that discharge in response to the somesthetic stimuli during the categorization task. Those neurons that respond irrespective of the stimulus speed appear to be involved in the general sensorimotor behavior of the animal during the execution of the task. The results suggest that the putamen may play a role in bimanual tasks. The recording of neurons in the right and left putamen whose activities correlate with the speed categories suggests that this region of the basal ganglia, in addition to its role in motor functions, is also involved in the animal's decision process.

Categorization of somaesthetic stimuli: sensorimotor performance and neuronal activity in primary somatic sensory cortex of awake monkeys.

We used psychometric techniques to study the sensorimotor performance of four monkeys trained to classify the speed of moving tactile stimuli. Animals performed the task by pressing one of two target switches to indicate whether the speed of probe movement across the glabrous skin of the hand was low or high. Psychometric curves indicated that animals classified the stimulus speeds irrespective of which finger was stimulated, traverse distance and direction. The mean values of the reaction (RT) and movement (MT) times during the correct categorization of low and high stimulus speeds were similar. However, a slight increase was detected in the mean values of the RT during the incorrect categorization but not in the MT. During the task, activity of single neurones (n = 45) was recorded in primary somatic sensory (SI) cortex. The results indicate that a class of neurones (n = 12) of SI cortex increased their impulse rates as a function of the stimulus speeds. However, the magnitude of their responses was similar during the correct and incorrect categorizations of stimuli. The same neurones also responded when the same set of stimuli used in the categorization task were delivered passively. Neurones of SI cortex responded with a latency of 25.8 +/- 0.6 ms (+/- s.e.m.) relative to the beginning of the moving tactile stimuli during the categorization task. The same neurones (n = 17) also responded with a similar latency (24.6 +/- 4.0 ms) when the stimuli were delivered passively. These results may suggest that, although this evoked neuronal activity may be important for the perception of the moving tactile stimuli, more central structures associated with SI cortex may determine the performance of this learned somaesthetic task.

Neuronal activity of primate putamen during categorical perception of somaesthetic stimuli.

We have studied neuronal activity in the putamen of two monkeys trained to discriminate the speed of moving tactile stimuli. Animals pressed one of two target switches to indicate whether the speed of the probe across the skin was low or high. The activity of single neurones was recorded in the putamen ipsilateral to the glabrous skin of the stimulated hand and contralateral to the responding arm. During the task, we recorded neurones in the putamen that showed responses confined exclusively to the stimulus period of all speeds. A second class of putamen neurones responded during the stimulus period but continued discharging during the reaction and movement time period. None of these two classes of putamen neurones discharged when the same set of stimuli were delivered passively. A third class of putamen neurones responded differentially in the discrimination task and predicted whether the speed of the stimulus was low or high. A number of these neurones, which responded differentially during the categorization task, were tested in a light instruction task. This tested the possibility that these differential responses were associated with the intention to move the arm to one of the two target switches. Few neurones responded in this situation. These results indicate that the putamen, in addition to its role in motor regulation, is also involved in higher order aspects of sensory-motor behaviour and in the sensory decision process in this learned somaesthetic task.

Representation of tactile signals in primate supplementary motor area.

1. We have studied the neuronal activity in the supplementary motor area (SMA) of two monkeys who categorized the speed of moving tactile stimuli delivered to the glabrous skin of the hand ipsilateral to the site of cortical recording and contralateral to the responding arm. 2. A large number of SMA neurons responded to the stimuli of all speeds (176 of 522) but only when those stimuli controlled behavior. 3. A second class of SMA neurons responded differentially in the categorization task (35 during the stimuli and 51 during the reaction time period) and predicted its outcome. 4. To dissociate the interrupt target switches presses from the tactile categorization responses, sixteen neurons, which responded to the stimuli in all speeds, and 11 neurons, which discharged differentially, were tested in a visual control task. None of these two classes of neurons responded in this situation. 5. It is concluded that the SMA ipsilateral to sensory input and contralateral to the responding arm is involved in the sensory decision process in this somesthetic categorization task.

Turning behavior, barrel rolling, and sensory neglect induced by picrotoxin in the thalamus.

Microinjections of picrotoxin in the ventromedial thalamic nucleus (VMT) in the rat elicited a slow contralateral turning plus a stereotyped upward sniffing. The animals showed a tendency to stand on the hind legs, increased grooming, and a tilt of the head toward the injected side. Similar injections in the parafascicular nuclear complex (Pf) initiated a faster ipsilateral turning and all the behaviors described plus another motor component: an ipsilateral barrel rolling. A 6-OHDA lesion did not impair the barrel rolling induced by picrotoxin injection in the Pf nucleus. Animals injected with picrotoxin in the Pf and VMT showed a marked increase in the current needed to evoke an orienting response after stimulation of the contralateral flank. Unlike rats treated with 6-OHDA, this response to ipsilateral stimulation was also reduced.