How do monkeys view faces?—a study of eye movements

Face perception plays a crucial role in primate social communication. We have investigated the pattern of eye movements produced by rhesus monkeys (Macaca mulatta) as they viewed images of faces. Eye positions were recorded accurately using implanted eye coils, while neutral upright, inverted and scrambled images of monkey and human faces were presented on a computer screen. The monkeys exhibited a similar eye scan pattern while viewing familiar and unfamiliar monkey face images, or while viewing monkey and human face images. No differences were observed in the distribution of viewing times, number of fixations, time into the trial of first saccade to local facial features, and the temporal and spatial characteristics of viewing patterns across the facial images. However, there was a greater probability of re-fixation of the eye region of unfamiliar faces during the first few seconds of the trial suggesting that the eyes are important for the initial encoding of identity. Indeed, the highest fixation density was found in the eye region of all the face images. The viewing duration and the number of fixations per image decreased when inverted or scrambled faces were presented. The eye region in these modified images remained the primary area of fixation. However, the number of fixations directed to the eyes decreased monotonically from the upright images through the inverted versions to the scrambled face images. Nonetheless, the eyes remain the most salient facial substructure regardless of the arrangement of other features, although the extent of salience which they attain may depend both on the low level properties of the eyes and on the global arrangement of facial features. Electronic Publication     

Motor cortical activity in a memorized delay task

Summary Two rhesus monkeys were trained to move a handle on a two-dimensional (2D) working surface in directions specified by a light at the plane. They first captured with the handle a light on the center of the plane and then moved the handle in the direction indicated by a peripheral light (cue signal). The signal to move (go signal) was given by turning off the center light. The following tasks were used: (a) In the non-delay task the peripheral light was turned on at the same time as the center light went off. (b) In the memorized delay task the peripheral light stayed on for 300 ms and the center light was turned off 450–750 ms later. Finally, (c) in the non-memorized delay task the peripheral light stayed on continuously whereas the center light went off 750–1050 ms after the peripheral light came on. Recordings in the arm area of the motor cortex (N= 171 cells) showed changes in single cell activity in all tasks. In both delay tasks, the neuronal population vector calculated every 20 ms after the onset of the peripheral light pointed in the direction of the upcoming movement, which was instructed by the cue light. Moreover, the strength of the population signal showed an initial peak shortly after the cue onset in both the memorized and non-memorized delay tasks but it maintained a higher level during the memorized delay period, as compared to the non-memorized task. These results indicate that the motor cortex is involved in encoding and holding in memory directional information concerning a visually cued arm movement and that these processes can be visualized using neuronal population vector analysis.     

Excitability of reciprocal and recurrent inhibitory pathways after voluntary muscle relaxation in man

Summary We studied the potential contribution of postsynaptic mechanisms to the depression of reflex excitability which occurs immediately after a voluntary release from tonic muscle contraction. The excitability of the Soleus (Sol) motor pool was tested at rest and after voluntary muscle relaxation. In both cases the Sol H-reflex was conditioned by 1. a single shock to the peroneal nerve, in order to activate the Ia interneurones (INs) mediating the reciprocal inhibition via a peripheral input, or by 2. a short-lasting voluntary contraction of the Tibialis Anterior (TA) muscle, to activate the Ia INs via a central command. Changes in excitability of Renshaw cells were also tested at rest and after release, to assess the role of recurrent inhibition in the release-induced inhibition of the Sol H-reflex. It was demonstrated that: 1. the excitability of the INs mediating the reciprocal inhibition was only slightly enhanced in comparison with resting conditions; 2. the H-reflex of the antagonist muscle (TA) evoked after Sol release was not consistently facilitated with respect to rest; 3. the command to contract the TA muscle reduced the H-reflex of the Sol muscle during rest but not after Sol release; 4. recurrent inhibition did not increase its effect in the post-release period. Such features suggest that recurrent and reciprocal post-synaptic inhibitions do not play a major role in reducing the reflex excitability of a relaxing muscle; rather, the command to release prevents the reciprocal inhibitory effect which accompanies the contraction of the antagonist muscle. The findings support the concept that release-induced reflex depression is mediated mainly by presynaptic inhibition of autogenetic spindle afferences (Schieppati and Crenna 1984).Supported by Italian M.P.I.     

Cat red nucleus activity preceding movement depends on initiation conditions

Summary The activity of 98 Red Nucleus neurons was recorded in 3 cats operantly conditioned to perform a ballistic forelimb flexion movement triggered after a brief sound in a simple Reaction Time condition, or Delayed after the same sound in the presence of a tone cue. Fifty-eight task related neurons presented changes of activity in either one or both conditions. Forty-four of them were studied quantitatively and classified in 3 categories: 1) only 16% of the units presented similar changes of firing preceding the triggered or delayed movement; 2) most units (55%) presented different changes of activity in the two conditions: in the Delayed condition, the activation occurred earlier before the movement, and/or the change in magnitude was reduced or the pattern of activity was modified; 3) moreover, for 29% of the units, the change of activity observed before movement in the Reaction Time condition was severely reduced or even absent in the Delayed condition. For some of these neurons a building-up of activity was observed very early in the Reaction Time condition, during the preparatory period, well before the occurrence of the conditioned stimulus. These results show that the Red Nucleus activity preceding a movement is clearly dependent on its initiation conditions. The distinct patterns of unit firing observed in the Reaction Time condition and in the Delayed condition are tentatively related to the different preparation and initiation constraints determined by the behavioral conditions.     

Perceiving a stable world during active rotational and translational head movements

When a person moves through the world, the associated visual displacement of the environment in the opposite direction is not usually seen as external movement but rather as a changing view of a stable world. We measured the amount of visual motion that can be tolerated as compatible with the perception of moving within a stable world during active, sinusoidal, translational and rotational head movement. Head movements were monitored by means of a low-latency, mechanical head tracker and the information was used to update a helmet-mounted visual display. A variable gain was introduced between the head tracker and the display. Ten subjects adjusted this gain until the visual display appeared stable during sinusoidal yaw, pitch and roll head rotations and naso-occipital, inter-aural and dorso-ventral translations at 0.5 Hz. Each head movement was tested with movement either orthogonal to or parallel with gravity. A wide spread of gains was accepted as stable (0.8 to 1.4 for rotation and 1.1 to 1.8 for translation). The gain most likely to be perceived as stable was greater than that required by the geometry (1.2 for rotation; 1.4 for translation). For rotational motion, the mean gains were the same for all axes. For translation there was no effect of whether the movement was inter-aural (mean gain 1.6) or dorso-ventral (mean gain 1.5) and no effect of the relative orientation of the translation direction relative to gravity. However translation in the naso-occipital direction was associated with more closely veridical settings (mean gain 1.1) and narrower standard deviations than in other directions. These findings are discussed in terms of visual and non-visual contributions to the perception of an earth-stable environment during active head movement.     

Electrical activity in the prefrontal cortex specific to no-go reaction of conditioned hand movement with colour discrimination in the monkey

Summary Monkeys were trained to perform hand movements in a reaction time task with discrimination between positive (go) and negative (no-go) light signals, and field potentials in various cortical areas were recorded and analysed with chronically implanted cortical electrodes. As previously reported, areas such as the prefrontal, premotor and motor cortices were active in association with simple visually-initiated, reaction-time hand movements. The caudal part of the dorsal bank of the principal sulcus was found to be activated specifically on no-go trials during discrimination, and revealed a relatively sharp surface-negative, depth-positive potential. The potential appeared at a latency of 110–150 ms, which was 150–210 ms earlier than the movement onset on go trials. With reversal of the go and no-go signals, this potential was found to be recorded only on no-go trials, irrespective of the colour used for the stimulus. It is suggested that the activity in the dorsal bank of the principal sulcus is related to the judgement not to execute the movement and/or the suppression of motor execution.     

Studies on cortical field potentials recorded during learning processes of visually initiated hand movements in monkeys

Summary A monkey was trained to lift a lever by wrist extension in response to a light stimulus. During the learning process of the task over several months, field potentials related not only to the task performance but also to substitution and stimulation experiments were recorded with chronically implanted electrodes on the surface and at a depth of 2.5–3.0 mm in the prefrontal, premotor, motor and prestriate cortices. In the substitution experiment, an examiner lifted a lever for the monkey so that it was watching the light and rewarded without the hand movement. In the stimulation experiment, the same light stimulus was simply delivered to the monkey. In a naive monkey which lifted the lever independently of the stimulus, stimulus-locked potentials were evoked by the task experiment in those cortices except the motor cortex, but none was elicited by the substitution or stimulation experiment. In a welltrained monkey, the substitution and stimulation experiments induced almost the same potentials as those prior to the task movement in respective cortices except the motor cortex, in which the component of cerebellar-induced premovement potential was not observed during the substitution and stimulation experiments. At an intermediate stage of learning, the situation was intermediate between the naive and well-trained stages and most premovement potentials except those in the motor cortex were elicited by the substitution experiment in reduced sizes, but nothing by the stimulation experiment.The present study suggests that the neuronal circuits for the operantly conditioned movement are functionally organized and gradually consolidated in the learning process, and that the consolidation is made earlier for the circuit involving association and premotor cortices than the circuit including the motor cortex in the process. The circuit to the motor cortex via the cerebro-cerebellar interconnection is recruited only on the execution of movement.     

Functional modification of agonist-antagonist electromyographic activity for rapid movement inhibition

Subjects made a fast elbow extension movement to designated target in response to a go signal. In 45% of trials a stop signal was presented after the go signal, to which subjects were asked to stop the movement as rapidly as possible. The interstimulus interval (ISI), or time interval between the go and stop signals, was randomly varied between 0 and 200 ms. Electromyographic (EMG) activity was recorded from biceps brachii and triceps brachii. Subjects could sometimes completely inhibit initiation of the movements when the ISI was 0 ms, but could rarely do so when the ISI exceeded 100 ms. For responses that were initiated but stopped on the way, the amplitude of the movement decreased linearly as the time interval (=modification time) from the stop signal to EMG onset increased. The peak velocity increased linearly as the movement amplitude increased. This tendency was similar to those previously reported in step-tracking movements with various amplitudes. In spite of the similarity in the kinematics of the movement, the EMG pattern was different from that of step-tracking movement. While the initial agonist burst (AG1) decreased linearly after the modification time exceeded 100 ms, the antagonist burst (ANT) increased compared with the go trial for the modification time from 0 to 200 ms and decreased after the modification time exceeded 300 ms. This change of activation is analogous to functional modification of middle-latency reflex EMG response to load, or cutaneous perturbation. In conclusion, it is suggested that adaptive mechanisms, which would functionally modify the reflex responses, are also continuously working during voluntary movements in response to sudden changes in environmental information. Received: 3 November 1997 / Accepted: 3 February 1998     

Neurochemical correlates of sparing from motor deficits in rats depleted of striatal dopamine as weanlings

The behavioral and neurochemical effects of striatal DA depletions were investigated in rats lesioned as weanlings (Day 27) or as adults (250-300 g). Administration of 6-OHDA into the medial forebrain bundle resulted in comparably large (> or = 95%) depletions of tissue levels of DA in both age groups. As expected, rats depleted of DA as adults exhibited marked deficits in motoric behavior and body weight regulation that persisted for the 8 days of postsurgical observation. In contrast, rats depleted of DA as weanlings were spared from such deficits, and their behavior closely resembled that of age-matched controls. Microdialysis studies revealed dialysate levels of striatal DA that paralleled these age-dependent behavioral differences. At a time when age-related behavioral differences were still quite pronounced (5-6 days postsurgery), basal DA levels were reduced by 80% of control values in rats lesioned as adults whereas basal DA levels in rats lesioned as weanlings were unchanged relative to their controls. Finally, adults depleted of striatal DA as weanlings were no more sensitive to the movement-impairing effects of intrastriatal sulpiride (3.0 or 10.0 micrograms/hemisphere) infusions than were control rats. These data suggest that weanlings compensate for large, but incomplete, denervation of striatal DA with markedly enhanced release and turnover from residual terminals. This developmental plasticity may prevent the occurrence of behavioral deficits soon after the lesion and also the supersensitivity to the challenging effects of DA antagonists as animals grow into adulthood.     

Linearity,symmetry and additivity of the human eye-movement response to maintained unilateral and bilateral surface galvanic (DC) vestibular stimulation

Recent studies have shown that, although responses to long-duration, constant-current surface galvanic vestibular stimulation (GVS) show substantial interindividual variability, individual subjects show a reliable, repeatable, idiosyncratic oculomotor response pattern to GVS. It follows that GVS may be a more reliable stimulus than may have been anticipated from the literature. The aim of the present study was to examine the metrics of 3D eye-movement responses to maintained (120 s), unilateral and bilateral surface GVS. Eye movements were measured using computerised video-oculography. Two experiments were conducted: Experiment 1 examined whether the normal response is linear over increasing levels of current; and Experiment 2 examined (1) whether the normal response to surface GVS is symmetrical when comparing stimulated sides, (2) whether the normal response to surface GVS is symmetrical when the polarity of the stimulating current was reversed, and (3) whether there is additivity in the normal response to combinations of unilateral/bilateral surface GVS. Five subjects participated in Experiment 1 and eight subjects participated in Experiment 2. In both experiments, the onset of stimulation produced characteristic eye-movement responses: changes in torsional position with the upper pole of both eyes rolling towards the anode and away from the cathode; together with horizontal and torsional nystagmus with slow phases towards the anode and away from the cathode; and negligible vertical nystagmus. These responses reversed direction at stimulus offset. In the fixation condition of Experiment 1, the magnitude of ocular torsional position (OTP) and torsional nystagmus responses showed a linear relationship over conditions of increasing current strength, as did OTP, torsional and horizontal nystagmus responses in darkness. The results of Experiment 2 showed that responses to unilateral stimulation are symmetrical between stimulated sides, symmetrical between stimulating polarities, and additive (with respect to responses to bilateral stimulation). The principles derived from these findings, as well as those of recent studies, provide a foundation for future work investigating eye-movement responses to surface GVS in patients with known types of vestibular dysfunction. Electronic Publication