Unveiling the invisible: receivers use object weight cues for grip force planning in handover actions.

Handover actions are part of our daily lives. Whether it is the milk carton at the breakfast table or tickets at the box office, we usually perform these joint actions without much conscious attention. The individual actions involved in handovers, that have already been studied intensively at the level of individual actions, are grasping, lifting, and transporting objects. Depending on the object's properties, actors must plan their execution in order to ensure smooth and efficient object transfer. Therefore, anticipatory grip force scaling is crucial. Grip forces are planned in anticipation using weight estimates based on experience or visual cues. This study aimed to investigate whether receivers are able to correctly estimate object weight by observing the giver's kinematics. For this purpose, handover actions were performed with 20 dyads, manipulating the participant role (giver/receiver) and varying the size and weight of the object. Due to the random presentation of the object weight and the absence of visual cues, the participants were unaware of the object weight from trial to trial. Kinematics were recorded with a motion tracking system and grip forces were recorded with customized test objects. Peak grip force rates were used as a measure of anticipated object weight. Results showed that receiver kinematics are significantly affected by object weight. The peak grip force rates showed that receivers anticipate object weight, but givers not. This supports the hypothesis that receivers obtain information about the object weight by observing giver's kinematics and integrating this information into their own action execution.

Comparison of the classically conditioned withdrawal reflex in cerebellar patients and healthy control subjects during stance: 2. Biomechanical characteristics.

This study addresses cerebellar involvement in classically conditioned nociceptive lower limb withdrawal reflexes in standing humans. A preceding study compared electromyographic activities in leg muscles of eight patients with cerebellar disease (CBL) and eight age-matched controls (CTRL). The present study extends and completes that investigation by recording biomechanical signals from a strain-gauge-equipped platform during paired auditory conditioning stimuli (CS) and unconditioned stimuli (US) trials and during US-alone trials. The withdrawal reflex performance-lifting the stimulated limb (decreasing the vertical force from that leg, i.e. 'unloading') and transferring body weight to the supporting limb (increasing the vertical force from that leg, i.e. 'loading')-was quantified by the corresponding forces exerted onto the platform. The force changes were not simultaneous but occurred as a sequence of multiple force peaks at different times depending on the specific limb task (loading or unloading). Motor learning, expressed by the occurrence of conditioned responses (CR), is characterized by this sequence beginning already within the CSUS window. Loading and unloading were delayed and prolonged in CBL, resulting in incomplete rebalancing during the analysis period. Trajectory loops of the center of vertical pressure-derived from vertical forces-were also incomplete in CBL within the recording period. However, exposing CBL to a CS resulted in motor improvement reflected by shortening the time of rebalancing and by optimizing the trajectory loop. In summary, associative responses in CBL are not absent although they are less frequent and of smaller amplitude than in CTRL.

Comparison of the classically conditioned withdrawal reflex in cerebellar patients and healthy control subjects during stance: I. electrophysiological characteristics.

The aim of this study was to demonstrate the involvement of the human cerebellum in the classically conditioned lower limb withdrawal reflex in standing subjects. Electromyographic activity was recorded from the main muscle groups of both legs of eight patients with cerebellar disease (CBL) and eight control subjects (CTRL). The unconditioned stimulus (US) consisted of electrical stimulation of the tibial nerve at the medial malleolus. The conditioning stimulus (CS) was an auditory signal given via headphones. Experiments started with 70 paired conditioning stimulus-unconditioned stimulus(CSUS) trials followed by 50 US-alone trials. The general reaction consisted of lifting and flexing the stimulated (stepping) leg with accompanying activation of the contralateral (supporting) leg. In CTRL, the ipsilateral (side of stimulation) flexor and contralateral extensor muscles were activated characteristically. In CBL, the magnitudes of ipsilateral flexor and contralateral extensor muscle activation were reduced comparably. In CTRL, the conditioning process increased the incidence of conditioned responses (CR), following a typical learning curve, while CBL showed a clearly lower CR incidence with a marginal increase, albeit, at a shorter latency. Conditioning processes also modified temporal parameters by shortening unconditioned response (UR) onset latencies and UR times to peak and, more importantly in CBL, also the sequence of activation of muscles, which became similar to that of CTRL. The expression of this reflex in standing subjects showed characteristic differences in the groups tested with the underlying associative processes not being restricted exclusively to the CR but also modifying parameters of the innate UR.

Real-time supervisor system based on trinary logic to control experiments with behaving animals and humans.

A new method is presented based on trinary logic able to check the state of different control variables and synchronously record the physiological and behavioral data of behaving animals and humans. The basic information structure of the method is a time interval of defined maximum duration, called time slice, during which the supervisor system periodically checks the status of a specific subset of input channels. An experimental condition is a sequence of time slices subsequently executed according to the final status of the previous time slice. The proposed method implements in its data structure the possibility to branch like an if-else cascade and the possibility to repeat parts of it recursively like the while-loop. Therefore its data structure contains the most basic control structures of programming languages. The method was implemented using a real-time version of LabVIEW programming environment to program and control our experimental setup. Using this supervision system, we synchronously record four analog data channels at 500 Hz (including eye movements) and the time stamps of up to six neurons at 100 kHz. The system reacts with a resolution within 1 ms to changes of state of digital input channels. The system is set to react to changes in eye position with a resolution within 4 ms. The time slices, experimental conditions, and data are handled by relational databases. This facilitates the construction of new experimental conditions and data analysis. The proposed implementation allows continuous recording without an inter-trial gap for data storage or task management. The implementation can be used to drive electrophysiological experiments of behaving animals and psychophysical studies with human subjects.

Early- and late-responding cells to saccadic eye movements in the cortical area V6A of macaque monkey.

The cortical area V6A, located in the dorsal part of the anterior bank of the parieto-occipital sulcus, contains retino- and craniocentric visual neurones together with neurones sensitive to gaze direction and/or saccadic eye movements, somatosensory stimulation and arm movements. The aim of this work was to study the dynamic characteristics of V6A saccade-related activity. Extracellular recordings were carried out in six macaque monkeys performing a visually guided saccade task with the head restrained. The task was performed in the dark, in both the dark and light, and sometimes in the light only. The discharge of certain neurones during saccades is due to their responsiveness to visual stimuli. We used a statistical method to distinguish responses due to visual stimulation from those responsible for saccadic control. Out of 597 V6A neurones tested, 66 (11%) showed responses correlated with saccades; 26 of 66 responded also to visual stimulation and 31 of 66 did not; the remaining 9 were not visually tested. We calculated the response latency to saccade onset and its inter-trial variance in 24 of 66 neurones. Saccade neurones could respond before, during or after the saccade. Neurones responding before saccade-onset or during saccades had much higher latency variance than neurones responding after saccades. The early-responding cells had a mean latency (+/-SD) of -64+/-62 ms, while the late-responding cells a mean latency of +89+/-20 ms. The responses to saccadic eye movements were directionally sensitive and varied with the amplitude of the saccade. Responses of late-responding cells disappeared in complete darkness. We suggest that the activity of early-responding cells represents the intended saccadic eye movement or the shift of attention towards another part of the visual space, whereas that of late-responding cells is a visual response due to retinal stimulation during saccades.

'Arm-reaching' neurons in the parietal area V6A of the macaque monkey.

In previous experiments we have found that several cells of area V6A in the macaque superior parietal lobule were activated by small and stereotyped movements of the arms (C. Galletti, P. Fattori, D. F. Kutz & P. P. Battaglini, Eur. J. Neurosci., 1997, 9, 410). This behaviour was not accounted for by retinal information, nor by somatosensory inputs from the arms. We now want to investigate whether V6A neurons are modulated by purposeful movements aimed at reaching visual targets or targets located outside the field of view. V6A neuronal activity was collected while monkeys performed arm movements during an instructed-delay reaching task in darkness. The task required the animal to reach out for a visual target in the peripersonal space and to bring the hand back to its body. Quantitative analysis of neuronal activity carried out on 55 V6A neurons showed that: (i) the great majority of neurons (71%) was significantly modulated during the execution of arm movements; (ii) 30% of neurons were significantly modulated during preparation of reaching; and (iii) modulations during both execution and preparation of reaching occurred in the absence of any visual feedback and were not due to eye movements. V6A reach-related neurons could be useful in guiding the hand to reach its target with or without visual feedback.

The cortical connections of area V6: an occipito-parietal network processing visual information.

The aim of this work was to study the cortical connections of area V6 by injecting neuronal tracers into different retinotopic representations of this area. To this purpose, we first functionally recognized V6 by recording from neurons of the parieto-occipital cortex in awake macaque monkeys. Penetrations with recording syringes were performed in the behaving animals in order to inject tracers exactly at the recording sites. The tracers were injected into the central or peripheral field representation of V6 in different hemispheres. Irrespective of whether injections were made in the centre or periphery, area V6 showed reciprocal connections with areas V1, V2, V3, V3A, V4T, the middle temporal area /V5 (MT/V5), the medial superior temporal area (MST), the medial intraparietal area (MIP), the ventral intraparietal area (VIP), the ventral part of the lateral intraparietal area and the ventral part of area V6A (V6AV). No labelled cells or terminals were found in the inferior temporal, mesial and frontal cortices. The connections of V6 with V1, and with all the retinotopically organized prestriate areas, were organized retinotopically. The connection of V6 with MIP suggests a visuotopic organization for this latter. Labelling in V6A and VIP after either central or peripheral V6 injections was very similar in location and extent, as expected on the basis of the nonretinotopic organization of these areas. We suggest that V6 plays a pivotal role in the dorsal visual stream, by distributing the visual information coming from the occipital lobe to the sensorimotor areas of the parietal cortex. Given the functional characteristics of the cells of this network, we suggest that it could perform the fast form and motion analyses needed for the visual guiding of arm movements as well as their coordination with the eyes and the head.

Influence of arm movements on saccades in humans.

When reaching for an object we usually look at it before we touch it with the hand. This often unconscious eye movement prior to the arm movement allows guiding of the final part of the hand trajectory by visual feedback. We examined the temporal and spatial coordination of this control system by psychophysical measurements of eye and arm movements of naive human subjects looking or looking and pointing as fast as possible to visual targets in physical and virtual-reality setups. The reaction times of saccades to a step-displaced target were reduced, and the number of corrective saccades decreased, when the subject had to produce a corresponding simultaneous hand movement to the same target. The saccadic reaction time was increased when saccade and hand movement went in opposite directions. In a double-step task the reaction time for the second saccade was longer than for the first. Co-use of the hand leads to an additional increase of saccadic reaction time. Taken together this study shows an improvement in initial saccades if they are accompanied by hand movements to the same target. This effect might ensure that the reach target is foveated early and accurately enough to support the visual feedback control of the hand near the target. Longer reaction times for the second saccade to double-step displaced targets might reflect a saccadic refractory time intensified by simultaneous arm movements. These results are discussed in the light of recent findings from our laboratory on saccade- and reach-related neurons in the superior colliculus of macaque monkeys.

The cortical visual area V6: brain location and visual topography.

The brain location and topographical organization of the cortical visual area V6 was studied in five hemispheres of four awake macaque monkeys. Area V6 is located in the caudal aspect of the superior parietal lobule (SPL). It occupies a 'C'-shaped belt of cortex whose upper branch is in the depth of the parieto-occipital sulcus (POS) and lower one is in the depth of the medial parieto-occipital sulcus (POM), with the medial surface of the brain as a zone of junction between the two branches. Area V6 contains a topographically organized representation of the contralateral visual field up to an eccentricity of at least 80 degrees. The lower visual field representation is located dorsally, in the ventral part of POS, and the upper field ventrally, in the dorsal wall of POM. The representation of the horizontal meridian forms the posterior border of V6. It is adjacent to area V3 in POS as well as in the caudal part of POM, on the ventral convexity of the brain. The lower vertical meridian forms the anterior border of V6, adjacent to area V6A. The upper vertical meridian is in the depth of POM. The representation of the central visual field is not magnified relative to that of the periphery. The central visual field (below 20-30 degrees of eccentricity) is represented in the medial-most aspect of the annectant gyrus, in the lateral part of the posterior bank of POS. The visuotopic organization of area V6 suggests a role in the analysis of the flow field resulting from self-motion, in selecting targets during visual searching as well as in the control of arm-reaching movements towards non-foveated targets.

Brain location and visual topography of cortical area V6A in the macaque monkey.

The brain location, extent and functional organization of the cortical visual area V6A was investigated in macaque monkeys by using single cell recording techniques in awake, behaving animals. Six hemispheres of four animals were studied. Area V6A occupies a horseshoe-like region of cortex in the caudalmost part of the superior parietal lobule. It extends from the medial surface of the brain, through the anterior bank of the parieto-occipital sulcus, up to the most lateral part of the fundus of the same sulcus. Area V6A borders on areas V6 ventrally, PEc dorsally, PGm medially and MIP laterally. Of 1348 neurons recorded in V6A, 61% were visual and 39% non-visual in nature. The visual neurons were particularly sensitive to orientation and direction of movement of visual stimuli. The inferior contralateral quadrant was the most represented one. Visual receptive fields were also found in the inferior ipsilateral quadrant and in the upper visual field. Receptive fields were on average smaller in the lower visual field than in the upper one. Both central and peripheral parts of the visual field were represented. Large parts of the visual field were represented in small regions of area V6A, and the same regions of the visual field were re-represented many times in different parts of this area, without any apparent topographical order. The only reliable sign of retinotopic organization was the predominance of central representation dorsally and far periphery ventrally. The functional organization of area V6A is discussed in the view that this area could be involved in the control of reaching out and grasping objects.

Superior area 6 afferents from the superior parietal lobule in the macaque monkey.

Superior area 6 of the macaque monkey frontal cortex is formed by two cytoarchitectonic areas: F2 and F7. In the present experiment, we studied the input from the superior parietal lobule (SPL) to these areas by injecting retrograde neural tracers into restricted parts of F2 and F7. Additional injections of retrograde tracers were made into the spinal cord to define the origin of corticospinal projections from the SPL. The results are as follows: 1) The part of F2 located around the superior precentral dimple (F2 dimple region) receives its main input from areas PEc and PEip (PE intraparietal, the rostral part of area PEa of Pandya and Seltzer, [1982] J. Comp. Neurol. 204:196-210). Area PEip was defined as that part of area PEa that is the source of corticospinal projections. 2) The ventrorostral part of F2 is the target of strong projections from the medial intraparietal area (area MIP) and from the dorsal part of the anterior wall of the parietooccipital sulcus (area V6A). 3) The ventral and caudal parts of F7 receive their main parietal input from the cytoarchitectonic area PGm of the SPL and from the posterior cingulate cortex. 4) The dorsorostral part of F7, which is also known as the supplementary eye field, is not a target of the SPL, but it receives mostly afferents from the inferior parietal lobule and from the temporal cortex. It is concluded that at least three separate parietofrontal circuits link the superior parietal lobule with the superior area 6. Considering the functional properties of the areas that form these circuits, it is proposed that the PEc/PEip-F2 dimple region circuit is involved in controlling movements on the basis of somatosensory information, which is the traditional role proposed for the whole dorsal premotor cortex. The two remaining circuits appear to be involved in different aspects of visuomotor transformations.

Population coding of arm-movement-related neurons in and below the superior colliculus of Macaca mulatta.

It has been shown for the motor cortex of primates, that an arm trajectory is coded as a population vector formed by many neurons with activities correlated with arm movements. Recently, neurons in the primate superior colliculus that also display activities related to arm movements have been described. In the present paper we show that a subpopulation of this type of neuron is able to code for limb movement by the population vector. However, the cosine function cannot describe these neurons adequately. Rather the Fisher distribution yields a much better description of arm-movement-related cells in the superior colliculus.

Arm movement-related neurons in the visual area V6A of the macaque superior parietal lobule.

Area V6A is a cortical visual area located in the posterior face of the superior parietal lobule in the macaque monkey. It contains visual neurons as well as neurons not activated by any kind of visual stimulation. The aim of this study was to look for possible features able to activate these latter neurons. We tested 70 non-visual V6A neurons. Forty-three of them showed an arm movement-related neural discharge due to somatosensory stimulation and/or skeletomotor activity of the upper limbs of the animal. The arm movement-related neural discharge started before the onset of arm movement, often before the earliest electromyographic activity. Thus, although the discharge is probably supported by proprioceptive and tactile inputs it is not fully dependent on them. Arm movement-related neurons of area V6A seem to be well equipped for integrating motor signals related to arm movements with somatosensory signals evoked by those movements. Taking into account also the visual characteristics of V6A neurons, it seems likely that area V6A as a whole is involved in the visual guiding of reaching.