How is electrical stimulation of the brain experienced,and how can we tell? Selected considerations on sensorimotor function and speech

ABSTRACT

Electrical stimulation of the nervous system is a powerful tool for localizing and examining the function of numerous brain regions. Delivered to certain regions of the cerebral cortex, electrical stimulation can evoke a variety of first-order effects, including observable movements or an urge to move, or somatosensory, visual, or auditory percepts. In still other regions the subject may be oblivious to the stimulation. Often overlooked, however, is whether the subject is aware of the stimulation, and if so, how the stimulation is experienced by the subject. In this review of how electrical stimulation has been used to study selected aspects of sensorimotor and language function, we raise questions that future studies might address concerning the subjects’ second-order experiences of intention and agency regarding evoked movements, of the naturalness of evoked sensory percepts, and of other qualia that might be evoked in the absence of an overt first-order experience.     

New method to identify nociceptor units innervating glabrous skin of the human hand

Summary A new technique is described for detecting nociceptor activity in microelectrode recordings from cutaneous fascicles of the human median nerve. The search strategy involves combined intraneural microstimulation and microneurographic recording in intrafascicular sites, where a critically low electrical stimulus amplitude evokes a threshold sensation of pain. From the subject's projection of pain to a small area of skin, the experimenter is guided to receptive fields of recordable nociceptor units. This technique has allowed, for the first time, to identify and study receptive properties of very high threshold nociceptors with A and C fibres in the glabrous skin of the human hand.     

重复电刺激前肢神经引起成年大鼠运动皮层的可塑性改变

为了了解成年大鼠运动皮层的功能可塑性，利用皮层内微刺激方法测定ＭＩ代表区并观察重复电刺激前肢神经对ＭＩ代表区的影响。实验组大鼠（９例）持续１．２－２小时的前肢神经电刺激导致前肢运动区与面部触须运动区边界向ＶＩ方向，移动２６３．３±９０．９μｍ并同时伴有运动阈值的改变；ＦＬ内ＭＴ降低５．０±１３．３μＡ，而在ＶＩ内ＭＴ升高９．６±１１．６μＡ对照组大鼠间隔１．５－２小时的两次测定结果，ＦＬ－ＶＩ边界     

Saliency-guided neural prosthesis for visual attention: Design and simulation

Recently the authors showed that a computational model of visual saliency could account for changes in gaze behavior of monkeys with damage in the primary visual cortex. Here we propose a neural prosthesis to restore eye gaze behavior by electrically stimulating the superior colliculus to drive visual attention. The saliency computational model is used to calculate the stimulation parameters from a real-time camera stream. Our simulations demonstrate that electrodes implanted in the superior colliculus at 1.0 mm spacing are, in principle, able to recover specifically those visual attention behaviors which are lost when the primary visual cortex is damaged.     

Delaying forelimb responses by microstimulation of macaque V1

Electrical microstimulation of macaque V1 has previously been shown to delay saccadic eye movements made to a punctate visual target placed in the receptive field of the stimulated neurons. It remains unclear whether this delay effect is specific to the oculomotor system or whether the effect can be demonstrated in the skeletomotor system as well. To address this question, a rhesus monkey was trained to depress a left or right lever with its respective hand in response to a visual target presented in the left or right hemifield. On 50% of trials, a 100 ms train of stimulation consisting of 100 μA, 0.2-ms anode-first pulses was delivered to the neurons before the onset of the visual target. Stimulation of V1 delayed the execution of the lever response when the visual target was positioned within the receptive field of the stimulated neurons. We suggest that the delay effect induced by microstimulation of V1 is largely due to a disruption of the visual signal as it is transmitted along the geniculostriate pathway.     

Mapping mesoscale cortical connectivity in monkey sensorimotor cortex with optical imaging and microstimulation

To map in vivo cortical circuitry at the mesoscale, we applied a novel approach to map interareal functional connectivity. Electrical intracortical microstimulation (ICMS) in conjunction with optical imaging of intrinsic signals (OIS) was used map functional connections in somatosensory cortical areas in anesthetized squirrel monkeys. ICMS produced activations that were focal and that displayed responses which were stimulation intensity dependent. ICMS in supragranular layers of Brodmann Areas 3b, 1, 2, 3a, and M1 evoked interareal activation patterns that were topographically appropriate and appeared consistent with known anatomical connectivity. Specifically, ICMS revealed Area 3b connections with Area 1; Area 1 connections with Areas 2 and 3a; Area 2 connections with Areas 1, 3a, and M1; Area 3a connections with Areas M1, 1, and 2; and M1 connections with Areas 3a, 1, and 2. These somatosensory connectivity patterns were reminiscent of feedforward patterns observed anatomically, although feedback contributions are also likely present. Further consistent with anatomical connectivity, intra-areal and intra-areal patterns of activation were patchy with patch sizes of 200–300 μm. In summary, ICMS with OIS is a novel approach for mapping interareal and intra-areal connections in vivo. Comparisons with feedforward and feedback anatomical connectivity are discussed.     

Differential effects of laminar stimulation of V1 cortex on target selection by macaque monkeys

We explored the effects of microstimulation on target selection by delivering stimulation at different depths within V1 (striate cortex) of the rhesus monkey (Macaca mulatta). Stimulation evoked saccadic eye movements that terminated in the receptive-field location of the activated neurons. The current thresholds for saccade evocation were highest (> or = 30 micro A) in the superficial layers and lowest (< or = 10 micro A) in the deep layers. To study target selection, one visual target was presented in the receptive-field location of the stimulated neurons and a second visual target was presented outside this location. Microstimulation delivered in concert with the appearance of the two targets decreased the probability that a monkey would select the target placed in the receptive-field location when the upper layers of V1 were stimulated, and it increased this probability when the lower layers were stimulated. We suggest that microstimulation of the upper layers of V1 disrupts visual signals from retina en route to higher cortical areas, whereas microstimulation of the lower layers activates V1 efferents that innervate the oculomotor system.     

Long-term motor cortex reorganization after facial nerve severing in newborn rats

Using the model of facial nerve injury, we have compared the effect of injury in newborn and adult rats on the adult rat motor cortex (M1). To this end, the facial nerve was severed in 10 newborn rats 2 days after birth (Newborn group) and in 10 adult rats (Adult group). In both the Control (contralateral to untouched nerve) and the Experimental (contralateral to severed nerve) hemisphere of each rat, the M1 output organization was assessed by intracortical microstimulation. Our findings demonstrated that: (i) there is no statistical difference in the percentage of movement sites and in current thresholds required to evoke movement in Control hemispheres between the Adult and Newborn groups of rats; (ii) in Adult Experimental hemispheres, neck sites expand in the medial part of the vibrissae representation more extensively than shown in Newborn Experimental hemispheres; (iii) in Newborn Experimental hemispheres eye sites expand in the medial part of the vibrissae representation more extensively than in Adult Experimental hemispheres (these sites overlap the cortical region where electrical stimulation evokes neck movement in Adult Experimental hemispheres) and (iv) in both Newborn and Adult Experimental hemispheres, forelimb sites expand similarly thereby overlapping the same cortical region, corresponding to the lateral part of the vibrissae representation. We conclude that, when the facial nerve injury is performed in the newborn rat, the pattern of movement representation differs from that obtained with the same lesion in the mature brain only in the frontal cortex corresponding to the medial part of the normal vibrissae representation.     

Influence of oro-facial sensory input on the output of the cortical masticatory area in the anesthetized rabbit

In order to study the role of sensory inputs to the cortical masticatory area (CMA) and plasticity in the CMA, the representation of sensory inputs and the change of sensory inputs and motor outputs in the CMA 16 days after trigeminal deafferentation in the rabbit were examined. Neuronal activity was recorded in response to mechanical and electrical stimulation of the oro-facial region and cortically-induced rhythmical jaw movements (CIRJMs) were analyzed. Cortical neurons with receptive fields in the deafferented region were not found in the CMA. However, the projection area of the intact lingual nerve extended both antero-posteriorly and medio-laterally in the CMA and included neurons with long latency responses to lingual nerve stimulation. In a previous study in the rabbit, CIRJMs were classified into two groups according to their similarity to normal masticatory patterns: one pattern resembled that occurring during the food transport stage (T-pattern), and the other resembled that occurring during the chewing stage (C-pattern). These two patterns of CIRJMs were evoked from different stimulation sites: T-patterns were induced from the dorsal CMA and C-patterns were induced from the ventral CMA. The relationship between the patterns of CIRJMs and the site of stimulation in the deafferented rabbits was similar to that observed in normal rabbits. This finding suggests that sensory inputs to the CMA may not directly influence the CMA motor outputs controlling jaw movements, despite a close spatial relationship between the input and output of this area.