Grasping without sight: insights from the congenitally blind

Sherpa Romeo green journal: open accessWe reach for and grasp different sized objects numerous times per day. Most of these movements are visually-guided, but some are guided by the sense of touch (i.e. haptically-guided), such as reaching for your keys in a bag, or for an object in a dark room. A marked right-hand preference has been reported during visually-guided grasping, particularly for small objects. However, little is known about hand preference for haptically-guided grasping. Recently, a study has shown a reduction in right-hand use in blindfolded individuals, and an absence of hand preference if grasping was preceded by a short haptic experience. These results suggest that vision plays a major role in hand preference for grasping. If this were the case, then one might expect congenitally blind (CB) individuals, who have never had a visual experience, to exhibit no hand preference. Two novel findings emerge from the current study: first, the results showed that contrary to our expectation, CB individuals used their right hand during haptically-guided grasping to the same extent as visually-unimpaired (VU) individuals did during visually-guided grasping. And second, object size affected hand use in an opposite manner for haptically- versus visually-guided grasping. Big objects were more often picked up with the right hand during hapticallyguided, but less often during visually-guided grasping. This result highlights the different demands that object features pose on the two sensory systems. Overall the results demonstrate that hand preference for grasping is independent of visual experience, and they suggest a left-hemisphere specialization for the control of grasping that goes beyond sensory modalityYe

The causal role of three frontal cortical areas in grasping

Efficient object grasping requires the continuous control of arm and hand movements based on visual information. Previous studies have identified a network of parietal and frontal areas that is crucial for the visual control of prehension movements. Electrical microstimulation of 3D shape-selective clusters in AIP during fMRI activates areas F5a and 45B, suggesting that these frontal areas may represent important downstream areas for object processing during grasping, but the role of area F5a and 45B in grasping is unknown. To assess their causal role in the frontal grasping network, we reversibly inactivated 45B, F5a and F5p during visually-guided grasping in macaque monkeys. First, we recorded single neuron activity in 45B, F5a and F5p to identify sites with object responses during grasping. Then, we injected muscimol or saline to measure the grasping deficit induced by the temporary disruption of each of these three nodes in the grasping network. The inactivation of all three areas resulted in a significant increase in the grasping time in both animals, with the strongest effect observed in area F5p. These results not only confirm a clear involvement of F5p, but also indicate causal contributions of area F5a and 45B in visually-guided object grasping

The Causal Role of Three Frontal Cortical Areas in Grasping

Efficient object grasping requires the continuous control of arm and hand movements based on visual information. Previous studies have identified a network of parietal and frontal areas that is crucial for the visual control of prehension movements. Electrical microstimulation of 3D shape-selective clusters in AIP during functional magnetic resonance imaging activates areas F5a and 45B, suggesting that these frontal areas may represent important downstream areas for object processing during grasping, but the role of area F5a and 45B in grasping is unknown. To assess their causal role in the frontal grasping network, we reversibly inactivated 45B, F5a, and F5p during visually guided grasping in macaque monkeys. First, we recorded single neuron activity in 45B, F5a, and F5p to identify sites with object responses during grasping. Then, we injected muscimol or saline to measure the grasping deficit induced by the temporary disruption of each of these three nodes in the grasping network. The inactivation of all three areas resulted in a significant increase in the grasping time in both animals, with the strongest effect observed in area F5p. These results not only confirm a clear involvement of F5p, but also indicate causal contributions of area F5a and 45B in visually guided object grasping

Effect of viewing distance on object responses in macaque areas 45B, F5a and F5p

To perform real-world tasks like grasping, the primate brain has to process visual object information so that the grip aperture can be adjusted before contact with the object is made. Previous studies have demonstrated that the posterior subsector of the Anterior Intraparietal area (pAIP) is connected to frontal area 45B, and the anterior subsector of AIP (aAIP) to F5a (Premereur et al., 2015). However, the role of area 45B and F5a in visually-guided object grasping is poorly understood. Here, we investigated the role of area 45B, F5a and F5p in visually-guided grasping. If a neuronal response to an object during passive fixation represents the activation of a motor command related to the preshaping of the hand, such neurons should prefer objects presented within reachable distance. Conversely, neurons encoding a pure visual representation of an object should be less affected by viewing distance. Contrary to our expectations, we found that the majority of neurons in area 45B were object- and viewing distance selective, with a clear preference for the near viewing distance. Area F5a showed much weaker object selectivity compared to 45B, with a similar preference for objects presented at the Near position emerging mainly in the late epoch. Finally, F5p neurons were less object selective and frequently preferred objects presented at the Far position. Therefore, contrary to our expectations, neurons in area 45B - but not F5p neurons - prefer objects presented in peripersonal space

Effect of Terminal Haptic Feedback on the Sensorimotor Control of Visually and Tactile-Guided Grasping

When grasping a physical object, the sensorimotor system is able to specify grip aperture via absolute sensory information. In contrast, grasping to a location previously occupied by (no-target pantomime-grasp) or adjacent to (spatially dissociated pantomime-grasp) an object results in the specification of grip aperture via relative sensory information. It is important to recognize that grasping a physical object and pantomime-grasping differ not only in terms of their spatial properties but also with respect to the availability of haptic feedback. Thus, the objective of this dissertation was to investigate how terminal haptic feedback influences the underlying mechanisms that support goal-directed grasping in visual- and tactile-based settings. In Chapter Two I sought to determine whether absolute haptic feedback influences tactile-based cues supporting grasps performed to the location previously occupied by an object. Results demonstrated that when haptic feedback was presented at the end of the response absolute haptic signals were incorporated in grasp production. Such a finding indicates that haptic feedback supports the absolute calibration between a tactile defined object and the required motor output. In Chapter Three I examined whether haptic feedback influences the information supporting visually guided no-target pantomime-grasps in a manner similar to tactile-guided grasping. Results showed that haptic sensory signals support no-target pantomime-grasping when provided at the end of the response. Accordingly, my findings demonstrated that a visuo-haptic calibration supports the absolute specification of object size and highlights the role of multisensory integration in no-target pantomime-grasping. Importantly, however, Chapter Four demonstrated that a priori knowledge of haptic feedback is necessary to support the aforementioned calibration process. In Chapter Five I demonstrates that, unlike no-target pantomime-grasps, spatially dissociated pantomime-grasps precluded a visuo-haptic calibration. Accordingly, I propose that the top-down demands of decoupling stimulus-response relations in spatially dissociated pantomime-grasping renders aperture shaping via a visual percept that is immutable to the integration of haptic feedback. In turn, the decreased top-down demands of no-target pantomime-grasps allows haptic feedback to serve as a reliable sensory resource supporting an absolute visuo-haptic calibration

On-line control of grasping actions: object-specific motor facilitation requires sustained visual input

Dorsal stream visual processing is generally considered to underlie visually driven action, but when subjects grasp an object from memory, as visual information is not available, ventral stream characteristics emerge. In this study we use paired-pulse transcranial magnetic stimulation (TMS) to investigate the importance of the current visual input during visuomotor grasp. Previously, the amplitude of the paired-pulse motor evoked potentials (MEPs) in hand muscles before movement onset have been shown to predict the subsequent pattern of muscle activity during grasp. Specific facilitation of paired-pulse MEPs may reflect premotor–motor (PMC–M1) cortex connectivity. Here we investigate the paired-pulse MEPs evoked under memory-cued and visually driven conditions before grasping one of two possible target objects (a handle or a disc). All trials began with a delay period of 1200 ms. Then, a TMS pulse served as the cue to reach, grasp and hold the target object for 0.5 s. Total trial length was 5 s. Both objects were continually visible in both conditions, but the way in which the target object was designated differed between conditions. In the memory-cued condition, the target object was illuminated for the first 200 ms of the trial only. In the visually driven condition, the target object was illuminated throughout the 5 s trial. Thus, the conditions differed in whether or not the object to be grasped was designated at the time of movement initiation. We found that the pattern of paired-pulse MEP facilitation matched the pattern of object-specific muscle activity only for the visually driven condition. The results suggest that PMC–M1 connectivity contributes to action selection only when immediate sensory information specifies which action to make

Grasping the past: delay can improve visuomotor performance

“Optic ataxia” is caused by damage to the human posterior parietal cortex (PPC). It disrupts all components of a visually guided prehension movement, not only the transport of the hand toward an object's location [1], but also the in-flight finger movements pretailored to the metric properties of the object [2, 3 and 4]. Like previous cases [4 and 5], our patient (I.G.) was quite unable to open her handgrip appropriately when directly reaching out to pick up objects of different sizes. When first tested, she failed to do this even when she had previewed the target object 5 s earlier. Yet despite this deficit in “real” grasping, we found, counterintuitively, that I.G. showed good grip scaling when “pantomiming” a grasp for an object seen earlier but no longer present. We then found that, after practice, I.G. became able to scale her handgrip when grasping a real target object that she had previewed earlier. By interposing catch trials in which a different object was covertly substituted for the original object during the delay between preview and grasp, we found that I.G. was now using memorized visual information to calibrate her real grasping movements. These results provide new evidence that “off-line” visuomotor guidance can be provided by networks independent of the PPC

Exploring manual asymmetries during grasping: a dynamic causal modeling approach

Recording of neural activity during grasping actions in macaques showed that grasp-related sensorimotor transformations are accomplished in a circuit constituted by the anterior part of the intraparietal sulcus (AIP), the ventral (F5) and the dorsal (F2) region of the premotor area. In humans, neuroimaging studies have revealed the existence of a similar circuit, involving the putative homolog of macaque areas AIP, F5 and F2. These studies have mainly considered grasping movements performed with the right dominant hand and only a few studies have measured brain activity associated with a movement performed with the left non-dominant hand. As a consequence of this gap, how the brain controls for grasping movement performed with the dominant and the non-dominant hand still represents an open question. A functional resonance imaging experiment (fMRI) has been conducted, and effective connectivity (Dynamic Causal Modelling, DCM) was used to assess how connectivity among grasping-related areas is modulated by hand (i.e., left and right) during the execution of grasping movements towards a small object requiring precision grasping. Results underlined boosted inter-hemispheric couplings between dorsal premotor cortices during the execution of movements performed with the left rather than the right dominant hand. More specifically, they suggest that the dorsal premotor cortices may play a fundamental role in monitoring the configuration of fingers when grasping movements are performed by either the right and the left hand. This role becomes particularly evident when the hand less-skilled (i.e., the left hand) to perform such action is utilized. The results are discussed in light of recent theories put forward to explain how parieto-frontal connectivity is modulated by the execution of prehensile movements