Response of Anterior Parietal Cortex to Different Modes of Same-Site Skin Stimulation

1998 ◽  
Vol 80 (6) ◽  
pp. 3272-3283 ◽  
Author(s):  
M. Tommerdahl ◽  
K. A. Delemos ◽  
O. V. Favorov ◽  
C. B. Metz ◽  
C. J. Vierck ◽  
...  

Tommerdahl, M., K. A. Delemos, O. V. Favorov, C. B. Metz, C. J. Viereck, Jr., and B. L. Whitsel. Response of anterior parietal cortex to different modes of same-site skin stimulation. J. Neurophysiol. 80: 3272–3283, 1998. Intrinsic optical signal (IOS) imaging was used to study responses of the anterior parietal cortical hindlimb region (1 subject) and forelimb region (3 subjects) to repetitive skin stimulation. Subjects were four squirrel monkeys anesthetized with a halothane/nitrous oxide/oxygen gas mixtures. Cutaneous flutter of 25 Hz evoked a reflectance decrease in the sectors of cytoarchitectonic areas 3b and/or 1 that receive input from the stimulated skin site. The intrinsic signal evoked by 25-Hz flutter attained maximal intensity ≤2.5–3.5 s after stimulus onset, remained well maintained as long as stimulation was continued, and disappeared rapidly (usually ≤2–5 s) after stimulus termination. Repetitive skin heating stimuli were delivered via a probe/thermode in stationary contact with the skin (6 temperature ramps/trial; within-trial ramp frequency 0.42 Hz; intertrial interval 180 s; initial temperature 32–36°C; maximal temperature 48–52°C; rate of temperature change 19°C/s). Skin heating led to a large-amplitude reflectance decrease within a zone of area 3a, which neighbored the region in areas 3b/1 that emitted an intrinsic signal in response to same-site 25-Hz flutter in the same subject. In three of four subjects a lower-amplitude decrease in reflectance also occurred in a region of area 4 continuous with the area 3a region that responded maximally to same-site skin heating. The reflectance decrease evoked in areas 3a/4 by skin heating consistently exceeded in both intensity and spatial extent the decrease in reflectance evoked in areas 3b/1 by same-site 25-Hz cutaneous flutter. These findings are viewed as consistent with the proposal that area 3a plays a leading role in the anterior parietal cortical processing of the afferent drive evoked by skin-heating stimuli perceived as painful. In all four subjects the reflectance decrease evoked in areas 3a/4 by skin heating was accompanied by a simultaneous but opposite change in reflectance (a reflectance increase) within a large territory located immediately posterior to the regions that responded with a decrease in reflectance—an observation that raised the possibility that skin heating evoked opposing influences on the activity of area 3a and 3b/1 regions that receive input from the stimulated skin site. This was evaluated with the method of correlation mapping. The observations obtained with correlation mapping appear consistent with demonstrations by others that skin-heating stimuli perceived as painful by conscious subjects suppress/inhibit the anterior parietal response to innocuous mechanical skin stimulation. The opposing (relative to the response of area 3a) optical response of area 1 and/or area 3b during skin heating stimulation is attributed to suppression/inhibition of area 1 and/or area 3b neuron activity.

1999 ◽  
Vol 82 (1) ◽  
pp. 16-33 ◽  
Author(s):  
M. Tommerdahl ◽  
K. A. Delemos ◽  
B. L. Whitsel ◽  
O. V. Favorov ◽  
C. B. Metz

The response of anesthetized squirrel monkey anterior parietal (SI) cortex to 25 or 200 Hz sinusoidal vertical skin displacement stimulation was studied using the method of optical intrinsic signal (OIS) imaging. Twenty-five-Hertz (“flutter”) stimulation of a discrete skin site on either the hindlimb or forelimb for 3–30 s evoked a prominent increase in absorbance within cytoarchitectonic areas 3b and 1 in the contralateral hemisphere. This response was confined to those area 3b/1 regions occupied by neurons with a receptive field (RF) that includes the stimulated skin site. In contrast, same-site 200-Hz stimulation (“vibration”) for 3–30 s evoked a decrease in absorbance in a much larger territory (most frequently involving areas 3b, 1, and area 3a, but in some subjects area 2 as well) than the region that undergoes an increase in absorbance during 25-Hz flutter stimulation. The increase in absorbance evoked by 25-Hz flutter developed quickly and remained relatively constant for as long as stimulation continued (stimulus duration never exceeded 30 s). At 1–3 s after stimulus onset, the response to 200-Hz stimulation, like the response to 25-Hz flutter, consisted of a localized increase in absorbance limited to the topographically appropriate region of area 3b and/or area 1. With continuing 200-Hz stimulation, however, the early response declined, and by 4–6 s after stimulus onset, it was replaced by a prominent and spatially extensive decrease in absorbance. The spike train responses of single quickly adapting (QA) neurons were recorded extracellularly during microelectrode penetrations that traverse the optically responding regions of areas 3b and 1. Onset of either 25- or 200-Hz stimulation at a site within the cutaneous RF of a QA neuron was accompanied by a substantial increase in mean spike firing rate. With continued 200-Hz stimulation, however, QA neuron mean firing rate declined rapidly (typically within 0.5–1.0 s) to a level below that recorded at the same time after onset of same-site 25-Hz stimulation. For some neurons, the mean firing rate after the initial 0.5–1 s of an exposure to 200-Hz stimulation of the RF decreased to a level below the level of background (“spontaneous”) activity. The decline in both the stimulus-evoked increases in absorbance in areas 3b/1 and spike discharge activity of area 3b/1 neurons within only a few seconds of the onset of 200-Hz skin stimulation raised the possibility that the predominant effect of continuous 200-Hz stimulation for >3 s is inhibition of area 3b/1 QA neurons. This possibility was evaluated at the neuronal population level by comparing the intrinsic signal evoked in areas 3b/1 by 25-Hz skin stimulation to the intrinsic signal evoked by a same-site skin stimulus containing both 25- and 200-Hz sinusoidal components (a “complex waveform stimulus”). Such experiments revealed that the increase in absorbance evoked in areas 3b/1 by a stimulus having both 25- and 200-Hz components was substantially smaller (especially at times >3 s after stimulus onset) than the increase in absorbance evoked by “pure” 25-Hz stimulation of the same skin site. It is concluded that within a brief time (within 1–3 s) after stimulus onset, 200-Hz skin stimulation elicits a powerful inhibitory action on area 3b/1 QA neurons. The findings appear generally consistent with the suggestion that the activity of neurons in cortical regions other than areas 3b and 1 play the leading role in the processing of high-frequency (≥200 Hz) vibrotactile stimuli.


1996 ◽  
Vol 75 (6) ◽  
pp. 2662-2670 ◽  
Author(s):  
M. Tommerdahl ◽  
K. A. Delemos ◽  
C. J. Vierck ◽  
O. V. Favorov ◽  
B. L. Whitsel

1. The response of anterior parietal cortex to skin stimuli was evaluated with optical intrinsic signal imaging and extracellular microelectrode recording methods in anesthetized squirrel monkeys. 2. Nonnoxious mechanical stimulation (vibrotactile or skin tapping) of the contralateral radial interdigital pad was accompanied by a decrease in reflectance (at 833 nm) in sectors of cytoarchitectonic areas 3b and 1. This intrinsic signal was in register with regions shown by previous receptive field mapping studies to receive low-threshold mechanoreceptor input from the radial interdigital pad. 3. A skin-heating stimulus applied to the contralateral radial interdigital pad with a stationary probe/thermode evoked no discernable intrinsic signal in areas 3b and 1, but evoked a signal within a circumscribed part of area 3a. The region of area 3a responsive to skin heating with the stationary probe/thermode was adjacent to the areas 3b and 1 regions that developed an intrinsic signal in response to vibrotactile stimulation of the same skin site. Skin heating with a stationary probe/thermode also evoked intrinsic signal in regions of areas 4 and 2 neighboring the area 3b/1 regions activated by vibrotactile stimulation of the contralateral radial interdigital pad. 4. The intrinsic signal evoked in area 3a by a series of heating stimuli to the contralateral radial interdigital pad (applied with a stationary probe/thermode) increased progressively in magnitude with repeated stimulation (exhibited slow temporal summation) and remained above prestimulus levels for a prolonged period after termination of repetitive stimulation. 5. Brief mechanical stimuli (,taps”) applied to the contralateral radial interdigital pad with a probe/thermode maintained either at 37 degrees C or at 52 degrees C were accompanied by the development of an intrinsic signal in both area 3a and areas 3b/1. For the 52 degrees C stimulus, the area 3a intrinsic signal was larger and the intrinsic signal in areas 3b/1 smaller than the corresponding signals evoked by the 37 degrees C stimulus. 6. Spike discharge activity was recorded from area 3a neurons during a repetitive heating stimulus applied with a stationary probe/ thermode to the contralateral radial interdigital pad. Like the area 3a intrinsic signal elicited by repetitive heating of the same skin site, the area 3a neuron spike discharge activity also exhibited slow temporal summation and poststimulus response persistence. 7. The experimental findings suggest 1) a leading role for area 3a in the anterior parietal cortical processing of skin-heating stimuli, and 2) the presence of inhibitory interactions between the anterior parietal responses to painful and vibrotactile stimuli consistent with those demonstrated in recent cortical imaging and psychophysical studies of human subjects.


1992 ◽  
Vol 68 (2) ◽  
pp. 518-527 ◽  
Author(s):  
T. P. Pons ◽  
P. E. Garraghty ◽  
M. Mishkin

1. Selective ablations of the hand representations in postcentral cortical areas 3a, 3b, 1, and 2 were made in different combinations to determine each area's contribution to the responsivity and modality properties of neurons in the hand representation in SII. 2. Ablations that left intact only the postcentral areas that process predominantly cutaneous inputs (i.e., areas 3b and 1) yielded SII recording sites responsive to cutaneous stimulation and none driven exclusively by high-intensity or "deep" stimulation. Conversely, ablations that left intact only the postcentral areas that process predominantly deep receptor inputs (i.e., areas 3a and 2) yielded mostly SII recording sites that responded exclusively to deep stimulation. 3. Ablations that left intact only area 3a or only area 2 yielded substantial and roughly equal reductions in the number of deep receptive fields in SII. By contrast, ablations that left intact only area 3b or only area 1 yielded unequal reductions in the number of cutaneous receptive fields in SII: a small reduction when area 3b alone was intact but a somewhat larger one when only area 1 was intact. 4. Finally, when the hand representation in area 3b was ablated, leaving areas 3a, 1, and 2 fully intact, there was again a substantial reduction in the encounter rate of cutaneous receptive fields. 5. The partial ablations often led to unresponsive sites in the SII hand representation. In SII representations other than of the hand no such unresponsive sites were found and there were no substantial changes in the ratio of cutaneous to deep receptive fields, indicating that the foregoing results were not due to long-lasting postsurgical depression or effects of anesthesia. 6. The findings indicate that modality-specific information is relayed from postcentral cortical areas to SII along parallel channels, with cutaneous inputs transmitted via areas 3b and 1, and deep inputs via areas 3a and 2. Further, area 3b provides the major source of cutaneous input to SII, directly and perhaps also via area 1. 7. The results are in line with accumulating anatomic and electrophysiologic evidence pointing to an evolutionary shift in the organization of the somatosensory system from the general mammalian plan, in which tactile information is processed in parallel in SI and SII, to a new organization in higher primates in which the processing of tactile information proceeds serially from SI to SII. The presumed functional advantages of this evolutionary shift are unknown.


2011 ◽  
Vol 106 (2) ◽  
pp. 722-730 ◽  
Author(s):  
Ulf Baumgärtner ◽  
Hagen Vogel ◽  
Shinji Ohara ◽  
Rolf-Detlef Treede ◽  
Fred Lenz

The cortical potentials evoked by cutaneous application of a laser stimulus (laser evoked potentials, LEP) often include potentials in the primary somatic sensory cortex (S1), which may be located within the subdivisions of S1 including Brodmann areas 3A, 3B, 1, and 2. The precise location of the LEP generator may clarify the pattern of activation of human S1 by painful stimuli. We now test the hypothesis that the generators of the LEP are located in human Brodmann area 1 or 3A within S1. Local field potential (LFP) source analysis of the LEP was obtained from subdural grids over sensorimotor cortex in two patients undergoing epilepsy surgery. The relationship of LEP dipoles was compared with dipoles for somatic sensory potentials evoked by median nerve stimulation (SEP) and recorded in area 3B (see Baumgärtner U, Vogel H, Ohara S, Treede RD, Lenz FA. J Neurophysiol 104: 3029–3041, 2010). Both patients had an early radial dipole in S1. The LEP dipole was located medial, anterior, and deep to the SEP dipole, which suggests a nociceptive dipole in area 3A. One patient had a later tangential dipole with positivity posterior, which is opposite to the orientation of the SEP dipole in area 3B. The reversal of orientations between modalities is consistent with the cortical surface negative orientation resulting from superficial termination of thalamocortical neurons that receive inputs from the spinothalamic tract. Therefore, the present results suggest that the LEP may result in a radial dipole consistent with a generator in area 3A and a putative later tangential generator in area 3B.


2002 ◽  
Vol 88 (1) ◽  
pp. 422-437 ◽  
Author(s):  
Anne J. Blood ◽  
Nader Pouratian ◽  
Arthur W. Toga

Characterization of neurovascular relationships is critical to accurate interpretation of functional neuroimaging data. We have previously observed spatial uncoupling of optical intrinsic signal imaging (OIS) and evoked potential (EP) responses in rodent barrel cortex following simultaneous whisker and forelimb stimulation, leading to changes in OIS response magnitude. To further test the hypothesis that this uncoupling may have resulted from “passive” overspill of perfusion-related responses between functional regions, we conducted the present study using temporally staggered rather than simultaneous whisker and forelimb stimulation. This paradigm minimized overlap of neural responses in barrel cortex and forelimb primary somatosensory cortex (SI), while maintaining overlap of vascular response time courses between regions. When contrasted with responses to 1.5-s lone-whisker stimulation, staggered whisker and forelimb stimulation resulted in broadening of barrel cortex OIS response time course in the temporal direction of forelimb stimulation. OIS response peaks were also temporally shifted toward the forelimb stimulation period; time-to-peak was shorter (relative to whisker stimulus onset) when forelimb stimulation preceded whisker stimulation and longer when forelimb stimulation followed whisker stimulation. In contrast with OIS and EP magnitude decreases previously observed during simultaneous whisker/forelimb stimulation, barrel cortex OIS response magnitude increased during staggered stimulation and no detectable changes in underlying EP activity were observed. Spatial extent of barrel cortex OIS responses also increased during staggered stimulation. These findings provide further evidence for spatial uncoupling of OIS and EP responses, and emphasize the importance of temporal stimulus properties on the effects of this uncoupling. It is hypothesized that spatial uncoupling is a result of passive overspill of perfusion-related responses into regions distinct from those which are functionally active. It will be important to consider potential influences of this uncoupling when designing and interpreting functional imaging studies that use hemodynamic responses to infer underlying neural activity.


1998 ◽  
Vol 79 (4) ◽  
pp. 2119-2148 ◽  
Author(s):  
Christian Xerri ◽  
Michael M. Merzenich ◽  
Bret E. Peterson ◽  
William Jenkins

Xerri, Christian, Michael M. Merzenich, Bret E. Peterson, and William Jenkins. Plasticity of primary somatosensory cortex paralleling sensorimotor skill recovery from stroke in adult monkeys. J. Neurophysiol. 79: 2119–2148, 1998. Adult owl and squirrel monkeys were trained to master a small-object retrieval sensorimotor skill. Behavioral observations along with positive changes in the cortical area 3b representations of specific skin surfaces implicated specific glabrous finger inputs as important contributors to skill acquisition. The area 3b zones over which behaviorally important surfaces were represented were destroyed by microlesions, which resulted in a degradation of movements that had been developed in the earlier skill acquisition. Monkeys were then retrained at the same behavioral task. They could initially perform it reasonably well using the stereotyped movements that they had learned in prelesion training, although they acted as if key finger surfaces were insensate. However, monkeys soon initiated alternative strategies for small object retrieval that resulted in a performance drop. Over several- to many-week-long period, monkeys again used the fingers for object retrieval that had been used successfully before the lesion, and reacquired the sensorimotor skill. Detailed maps of the representations of the hands in SI somatosensory cortical fields 3b, 3a, and 1 were derived after postlesion functional recovery. Control maps were derived in the same hemispheres before lesions, and in opposite hemispheres. Among other findings, these studies revealed the following 1) there was a postlesion reemergence of the representation of the fingertips engaged in the behavior in novel locations in area 3b in two of five monkeys and a less substantial change in the representation of the hand in the intact parts of area 3b in three of five monkeys. 2) There was a striking emergence of a new representation of the cutaneous fingertips in area 3a in four of five monkeys, predominantly within zones that had formerly been excited only by proprioceptive inputs. This new cutaneous fingertip representation disproportionately represented behaviorally crucial fingertips. 3) There was an approximately two times enlargement of the representation of the fingers recorded in cortical area 1 in postlesion monkeys. The specific finger surfaces employed in small-object retrieval were differentially enlarged in representation. 4) Multiple-digit receptive fields were recorded at a majority of emergent, cutaneous area 3a sites in all monkeys and at a substantial number of area 1 sites in three of five postlesion monkeys. Such fields were uncommon in area 1 in control maps. 5) Single receptive fields and the component fields of multiple-digit fields in postlesion representations were within normal receptive field size ranges. 6) No significant changes were recorded in the SI hand representations in the opposite (untrained, intact) control hemisphere. These findings are consistent with “substitution” and “vicariation” (adaptive plasticity) models of recovery from brain damage and stroke.


2016 ◽  
Vol 36 (12) ◽  
pp. 2051-2057 ◽  
Author(s):  
Edgar Santos ◽  
Fiorella León ◽  
Humberto Silos ◽  
Renan Sanchez-Porras ◽  
C William Shuttleworth ◽  
...  

The aim was to characterize the effects of magnesium sulfate, using i.v. bolus and local administration, using intrinsic signal imaging, and on electrocorticographic activity during the induction and propagation of spreading depolarizations in the gyrencephalic porcine brain. Local application of magnesium sulfate led to a complete inhibition of spreading depolarizations. One hour after washing out the topical magnesium sulfate, re-incidence of the spreading depolarizations was observed in 50% of the hemispheres. Those spreading depolarizations showed attenuation in hemodynamic characteristics and speed in intrinsic optical signal imaging. The electrical amplitude decreased through electrocorticographic activity. Intravenous magnesium therapy showed no significant effects on spreading depolarization incidence and characteristics.


2003 ◽  
Vol 90 (1) ◽  
pp. 143-154 ◽  
Author(s):  
Shin-Ichi Ito ◽  
A. D. (Bud) Craig

Penfield's sensory homunculus included visceral organs at its lateral extreme, and vagal input was recently identified lateral to the intraoral representation in primary somatosensory cortex (S1) of rats. We tested whether vagal input is similarly located in cats where area 3b (equivalent to S1) is clearly distinguishable from adjacent regions. Field potentials were recorded from the intact dura over the left hemisphere using electrical stimulation of the left or right cervical vagus nerve in seven cats. A surface positive-negative potential was evoked from either side in the lateral part of the sigmoid gyrus. Finer mapping made at the pial surface with a microelectrode identified a focal site anteromedial to the anterior tip of the coronal sulcus. Depth recordings demonstrated polarity reversals and multi-unit vagal responses, indicating that the potentials were generated by an afferent activation focus in the middle layers of the cortex. The S1 mechanoreceptive representation was localized by mapping multi-unit somatosensory receptive fields in the middle cortical layers near the coronal sulcus. The vagal-evoked potential site was distinctly anterior to the intraoral S1 representation and adjacent to the masseteric-nerve-evoked potential focus. Lesions made at the focal site revealed that this site is cytoarchitectonically located in area 3a not area 3b. Thus vagal input to the sensorimotor cortex in cats resembles deep rather than cutaneous somatic input, similar to the localization of nociceptive-specific input to area 3a in monkeys. The possibilities are considered that this vagal input is involved in motor control and in the sensory experience of visceral afferent activity.


1999 ◽  
Vol 19 (3) ◽  
pp. 246-259 ◽  
Author(s):  
Masahito Nemoto ◽  
Yasutomo Nomura ◽  
Chie Sato ◽  
Mamoru Tamura ◽  
Kiyohiro Houkin ◽  
...  

The origins of reflected light changes associated with neuronal activity (optical signals) were investigated in rat somatosensory cortex with optical imaging, microspectrophotometry, and laser-Doppler flowmetry, and dynamic changes in local hemoglobin concentration and oxygenation were focused on. Functional activation was carried out by 2-second, 5-Hz electrical stimulation of the hind limb under chloralose anesthesia. These measurements were performed at the contralateral parietal cortex through a thinned skull. Regional cortical blood flow (rCBF) started to rise 1.5 seconds after the stimulus onset, peaked at 3.5 seconds (26.7% ± 9.7% increase over baseline), and returned to near baseline by 10 seconds. Optical signal responses at 577, 586, and 805 nm showed a monophasic increase in absorbance coincident with the increase in rCBF; however, the signal responses at 605 and 760 nm were biphasic (an early increase and late decrease in absorbance) and microanatomically heterogeneous. The spectral changes of absorbance indicated that the concentrations of both total hemoglobin and oxyhemoglobin increased together with rCBF; deoxyhemoglobin, increased slightly but distinctly ( P = 0.016 at 1.0 seconds, P = 0.00038 at 1.5 seconds) just before rCBF increases, then decreased. The authors conclude that activity-related optical signals are greatly associated with a moment-to-moment adjustment of rCBF and metabolism to neuronal activity.


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