A. Berthoz

Reticulo-spinal neurons participating in the control of synergic eye and head movements during orienting in the cat

SummaryThe activity of 24 reticulo-spinal neurons (RSN) identified by antidromic stimulation at the C1-C2 level has been recorded intra-axonally in the pons of alert head-fixed cats during spontaneous gaze shifts and orienting towards novel targets. Relationship of neuronal discharge to saccadic eye movements, positions of fixation and EMG of dorsal neck muscles were analysed. The present report describes behavioral properties of a group of 14 RSN showing similar types of correlations with motor parameters during eye-head synergies. These “eye-neck” RSN (EN-RSN) generate bursts in synchrony with phasic components of ipsilateral neck EMG and leading ipsiversive saccades by a variable lead time. Bursts are followed by a prolonged discharge whose frequency decays even when eccentric eye position is maintained constant and accompanied by sustained neck muscle activity. The firing rate of EN-RSNs depends on eye position: they are silent with saccades in their ON-direction when the eyes are deviated towards the contralateral half of the oculomotor range and the ipsilateral neck muscles are relaxed. When the eyes cross the vertical meridian, the frequency of phasic and tonic components related to eye-head synergies increase proportionally to ipsilateral eye position. Ten of the 14 EN-RSNs, located in the pontine reticular formation, received monosynaptic input from the contralateral superior colliculus. Two were labeled by intra-axonal injection of HRP which revealed extensive branching in the abducens, facial, medial and lateral vestibular, prepositus and intercalatus nuclei and in the caudal pontine and bulbar reticular formation. It is concluded that the caudal pontine tegmentum, including the region just anterior to the abducens nucleus, contains RSNs whose signals seem appropriate to control phasic neck muscle activity and which also project to structures related to ocular and facial movements. Comparisons with the perisaccadic activity of tectal neurons projecting in the predorsal bundle reveals a profound transformation of the descending signal at the level of EN-RSNs which represent first order relay neurons of the tecto-reticulo-spinal pathway.

The contribution of otoliths and semicircular canals to the perception of two‐dimensional passive whole‐body motion in humans

1 Perception of two‐dimensional (2–D) whole‐body passive motion in the horizontal plane was studied in twelve blindfolded healthy volunteers: pure rotation in place (180 deg), linear motion (4.5 m) and a semicircular trajectory (radius, 1.5 m; angular acceleration, 0.2 rad s−2) were applied in random sequence by means of a remote‐controlled robot equipped with a racing‐car seat. The seat orientation in the horizontal plane was controlled by the experimenter, independent of the robot trajectory. Thus different degrees of otolith–canal interaction were obtained. The maximal linear acceleration during the semicircular trajectory was 0.1 g; however, the linear acceleration vector was complex as it rotated relative to the subjects head. 2 In the first of two sessions, subjects were instructed to maintain an angular pointer oriented towards a remote (15 m) previously seen target during the passive movements. In the second session they had to make a drawing of the path of the perceived trajectory, after the movement was finished. 3 The results showed that, on average, the movement of the pointer matched the dynamics of the rotatory component of the 2‐D motion well. This suggests that, in the range of linear accelerations used in this study, no appreciable influence of otolith input on canal‐mediated perception of angular motion occurred. 4 The curvature of the drawn paths was mostly explained by the input to the semicircular canals. Subjects’ reconstruction of motion did not account for the directional dynamics of the input to the otoliths occurring during passive motion. 5 This finding proves that reconstructing trajectory in space does not imply a mathematically perfect transformation of the linear and angular motion‐related inputs into a Cartesian or polar 2‐D representation. Physiological constraints on the interaction between motion direction and change of heading play an important role in motion perception.

Afferent neck projection to the cat cerebellar cortex.

Summary1.Afferent information from the neck plays an important role in the regulation of posture and the control of head and eye movements. The present series of experiments was designed in order to characterize the cerebellar projections of neck afferents in the cat. Both anesthetized and decerebrate animals were used, and recordings were obtained following electrical stimulation of the second cervical dorsal root (C2).2.Following electrical stimulation of C2 dorsal root, field potentials were recorded in lobules V and VI. Amplitude was maximum in the lateral third of the ipsilateral lobule V. These field potentials were produced by combined mossy and climbing fiber (MF and CF) volleys arriving at the cerebellar cortex with different latencies: 8 msec for MF and 24 msec for CF (mean values). The threshold for electrical stimulation was lower for MF than for CF activation; CF responses were evoked by high threshold afferents from muscle and joint receptors.3.A comparison was made between the latencies of cerebellar responses evoked by electrical stimulation of nuchal and other afferents (vestibular nerve, fore-and hindpaw). The latencies of MF responses vary widely, while those of the CF responses show a much smaller variation.4.Projection of the afferents from the neck was also demonstrated in the pars intermedia at the limit of the caudal folium of lobule V and of lobule VI (lobule simplex). A study of the convergence to this portion of pars intermedia demonstrated that stimulation of extraocular muscle nerves, trigeminal nerve, and fore-and hindpaws, as well as the neck afferents, generates a strong localized CF response with actual convergence onto single Purkinje cells. The recordings suggest that this area of wide convergence on CFs is not restricted to the superficial cortex, but extends through the depth of the fissura prima. Implications of these findings, in relation to the functional organization of lobule VI and the fissura prima, are discussed.

The role of inhibition in the hierarchical gating of executed and imagined movements

A theory is presented concerning the neuronal mechanisms which may underlie the organisation of imagined versus executed movements. A review is first presented of previous theoretical and experimental evidence suggesting that the brain can use the same mechanisms for the imagination and the execution of movement. In particular the fact that adaptation of the vestibulo-ocular reflex can be obtained by pure mental effort and not solely by conflicting visual and vestibular cues has been suggestive of the fact that the brain could internally simulate conflicts and use the same adaptive mechanisms used when actual sensory cues were in conflict. The saccadic system is taken as a good model for the study of this question because the mechanisms which underlie saccade generation are now partially understood at different levels from the brain stem to the cortex. The central idea of the theory is based upon the fact that, in parallel with the excitatory mechanisms underlying saccade generation, several inhibitory mechanisms in cascade allow the selective modulation and blockage of saccades. Synaptic inhibition is therefore supposed to play a major role in a hierarchical selective gating of saccade execution not at one but at several levels allowing a variety of different types of imagined movements some involving only the higher levels some in which the execution is only blocked at the very immediate premotor level. But in all cases the theory proposes that imagination and execution have many mechanisms in common. PET data showing that indeed the same structures are activated in both types of movements support this idea although the final answer will have to be brought by neuronal data.

Role of the different frontal lobe areas in the control of the horizontal component of memory-guided saccades in man

Two paradigms of memory-guided saccades were studied in 14 patients with focal vascular lesions affecting either the frontal eye field (FEF), or the supplementary eye field (SEF) or Brodmanns area 46 in the prefrontal cortex (PFC), and in 13 age-matched control subjects. In the first paradigm, the subject had to remember the position of a visual target with the body immobile and, in the second, the position towards which gaze was directed before a body rotation, i.e. with a vestibular input. In control subjects, the percentage of error in saccade accuracy (horizontal component) was greater in the second than in the first paradigm (37% and 14% on average, respectively). Compared with controls, amplitude error was significantly increased in the FEF group for the first paradigm only, in the SEF group for the second paradigm only, and in the PFC group for both paradigms. These results are consistent with (1) the PFC providing an improvement in the utilization by the saccade system of the visual and vestibular signals used in the two paradigms, and (2) the FEF and SEF providing an improvement in the utilization of visual signals in the first paradigm and vestibular signals in the second paradigm, respectively. Furthermore, from these findings and experimental data, it may be hypothesized (1) that the PFC is a part of the network contributing to short-term memorization of both visual and vestibular signals, and (2) that the FEF and SEF control two different types of memory-guided saccades, with separate calculation modes to determine their amplitude.

The control of slow orienting eye movements by tectoreticulospinal neurons in the cat: behavior, discharge patterns and underlying connections.

The activity of tectoreticulospinal neurons (TRSN) during orienting gaze shifts was studied in alert, head-fixed cats by intra-axonal recordings. The scope of the study was to evaluate the role of this class of superior colliculus neurons in the generation of slow eye movements (drifts) which often follow main-sequence saccades and sometimes appear as an independent motor event of orienting. The parameters of such movements are described in the first part of the paper. The organization of underlying pathways in the lower brainstem has been studied by intra-axonal horseradish peroxidase (HRP) tracing. The mean amplitude of postsaccadic drifts (PSD) is 1.21° (SD 0.63), but it can eventually reach 6–8°. PSDs have mean velocity of 14.9°/s (SD 4.28) and mean duration of 104.2 ms (SD 50.8). These two parameters are positively correlated with PSD amplitude. The presence of PSDs is usually associated with an increased neck muscle activity on the side toward which the eyes move. The durations of these two motor events show a reliable positive correlation. PSDs appear to occur when gaze error persists after a saccade and a correction is attempted by means of a slow eye movement and a head turn. The durations of TRSN bursts are, on average, longer than the sum of the lead time and the saccade duration. Bursts associated with combinations of saccades and PSD are significantly longer than those recorded in the absence of PSDs. The probability of occurrence of PSDs is higher when firing of TRSNs continues after saccade termination. Such prolonged discharges usually coincide with a combination of PSDs and phasic activation of the neck electromyogram. The mean firing rate of TRSNs during PSDs is 62% of that during saccade-related portions of the burst and declines to 45% after the end of PSDs. According to its timing and intensity, postsaccadic firing of TRSNs is appropriate as a signal underlying slow, corrective eye movements and later portions of phasic neck muscle contractions during orienting. Intraaxonal HRP labeling showed that visuomotor TRSNs of the X type (n = 3) terminate in the abducens nucleus, with 145–331 boutons terminaux and en passant. Average bouton densities in the nucleus are lower than in the periabducens reticular formation, but higher than in more rostral paramedian pontine reticular formation (PPRF) regions. Terminal fields in the PPRF match the locations of “eye-neck” reticulospinal neurons (RSNs) and exitatory burst neurons. Termination densities comparable with those in the caudal PPRF are found also in the rostral nucleus reticularis gigantocellularis, which contains phasic RSNs (“neck bursters”) and inhibitory burst neurons. Morphological observations alone do not exclude firing rate modulation of abducens motoneurons through the monosynaptic tectal pathway. However, the available physiological data point to a major role of a multiple convergent connection involving the eye-neck RSNs. In conclusion, the signals of X type TRSNs, reinforced by parallel connection through RSNs, encode mainly the intended head movement. Collateral actions of these two populations may be sufficient to induce slow, orienting eye movements, independently of the burst output from the classic saccadic generator.

Sex, Lies And Virtual Reality

Do male and female brains differ with respect to spatial processing? Gender differences in spatial abilities as well as in cerebral organization have led to suggestions that the sex of subjects should be taken into account in neuroscience studies. Here we demonstrate gender differences in the response to a visuovestibular information conflict created by a deceptive virtual environment.

Geometry of the superior colliculus mapping and efficient oculomotor computation

Numerous brain regions encode variables using spatial distribution of activity in neuronal maps. Their specific geometry is usually explained by sensory considerations only. We provide here, for the first time, a theory involving the motor function of the superior colliculus to explain the geometry of its maps. We use six hypotheses in accordance with neurobiology to show that linear and logarithmic mappings are the only ones compatible with the generation of saccadic motor command. This mathematical proof gives a global coherence to the neurobiological studies on which it is based. Moreover, a new solution to the problem of saccades involving both colliculi is proposed. Comparative simulations show that it is more precise than the classical one.

Saccade‐vestibulo‐ocular reflex co‐operation and eye‐head uncoupling during orientation to flashed target.

1. Eye‐head co‐ordination in the horizontal plane was studied in four human subjects using two successive flashes in the same direction, either increasing in eccentricity (IE), or decreasing in eccentricity (DE). 2. Results showed that for both conditions, head movements preceded eye movements and were typically longer or followed by a slow gaze movement. This slow movement was due to a vestibulo‐ocular reflex gain of less than one. Gaze accuracy was achieved by small head movement adjustments. 3. Gaze movement to an IE stimulus had a staircase pattern, and to a DE stimulus, a pulse‐step pattern or one gaze saccade to the final flash eccentricity. 4. In some cases, however, in response to a DE stimulus, the eye and head movements were directed to different displacements (dissociation); i.e. the head movement started towards the first flash eccentricity with a concomitant eye saccade to the second flash eccentricity. When this occurred, gaze movement did not resemble a pulse‐step pattern. 5. It is suggested that non‐visually orienting gaze is driven mainly by head movement. Eye and head movements can be either tightly coupled or dissociated, depending on the stimulus pattern.

Effects of prolonged weightlessness on mental rotation of three-dimensional objects.

Previous experiments have suggested that the analysis of visual images could be a gravity-dependent process. We investigated this hypothesis using a mental rotation paradigm with pictures of three-dimensional objects during a 26-day orbital flight aboard the Soviet MIR station. The analysis of cosmonauts response times showed that the mental rotation task is not greatly impaired in weightlessness. On the contrary, there are indications of a facilitation as: (1) the average rotation time per degree was shorter inflight than on the ground; (2) this difference seemed to be particularly marked for stimuli calling for roll axis rotations. However several factors may be responsible for this difference which was not obvious in one subject. Further experiments will have to test if this effect is really due to exposure to microgravity.