Response of SI cortex to ipsilateral, contralateral and bilateral flutter stimulation in the cat
© Tommerdahl et al; licensee BioMed Central Ltd. 2005
Received: 25 February 2005
Accepted: 22 April 2005
Published: 22 April 2005
While SII cortex is considered to be the first cortical stage of the pathway that integrates tactile information arising from both sides of the body, SI cortex is generally not considered as a region in which neuronal response is modulated by simultaneous stimulation of bilateral (and mirror-image) skin sites.
Optical intrinsic signal imaging was used to evaluate the response of SI and SII in the same hemisphere to 25 Hz sinusoidal vertical skin displacement stimulation ("skin flutter") applied contralaterally, ipsilaterally, and bilaterally (simultaneously) to the central pads of the forepaws. A localized increase in absorbance in both SI and SII occurred in response to both contralateral and bilateral flutter stimulation. Ipsilateral flutter stimulation evoked a localized increase in absorbance in SII, but little or no change in SI absorbance. In the forepaw representational region of SI, however, bilateral stimulation of the central pads evoked a response substantially smaller (approximately 30–35% smaller) than the response to flutter stimulation of the contralateral central pad.
The finding that the response of SI cortex to bilateral central pad flutter stimulation is substantially smaller than the response evoked by a contralateral flutter stimulus, together with the recently published observation that a region located posteriorly in SII responds with a substantially larger response to a bilateral flutter stimulus than the response evoked from the contralateral central pad, lead us to propose that the SI activity evoked by contralateral skin stimulation is suppressed/inhibited (via corticocortical connections between SII and SI in the same hemisphere) by the activity a simultaneous ipsilateral skin stimulus evokes in posterior SII.
It is established that multiple fields/areas in each cerebral hemisphere are activated at short latency by stimuli that trigger spike discharge activity in skin mechanoreceptive afferents. Of these the most extensively studied is SI – a region which most investigators have come to regard as responsive solely (the major exception being the face region of SI) to tactile stimuli delivered to contralateral skin sites. In contrast, SII has long been known to be activated at short latency by mechanical stimulation of skin sites on both sides of the body midline. Although this differential responsivity of SI and SII to stimulation of contralateral vs. ipsilateral skin sites has been widely accepted for more than five decades (since the pioneering evoked potential mapping studies of C.N. Woolsey and colleagues; e.g. ), the contribution of SII activation to cortical tactile information processing remains unknown. Additionally, although SII is considered to be the first cortical stage of the pathway that integrates information arising from both sides of the body, SI is generally not considered as a cortical region in which ipsilateral inputs play a major role in bilateral integration of information across the body mid-line. It is known, however, that even the distal limb representational regions in SI receive axonal projections (via the corpus callosum) from SI neurons in the opposite hemisphere [2, 3].
Recently, we reported the results from experiments in which we obtained simultaneous observations of the activity evoked in both SI and SII in the same hemisphere of cat cerebral cortex by a 25 Hz sinusoidal vertical skin displacement stimulus ("skin flutter") applied contralaterally, ipsilaterally, or bilaterally to the central pads of the forepaws . Briefly summarized, a localized increase in absorbance in both SI and SII was evoked by contralateral and also by bilateral flutter stimulation. Ipsilateral flutter stimulation also evoked a localized increase in absorbance in SII, but only a weak or negligible increase in the forepaw region of SI. Interestingly, the region of SII that responded with an increase in absorbance to ipsilateral stimulation was 2–3 mm posterior to the region in which absorbance increased maximally in response to stimulation of the contralateral central pad. Furthermore, in the posterior SII region that yielded the largest response to ipsilateral stimulation of the central pad, the response to bilateral central pad stimulation approximated a linear summation of the SII responses to independent stimulation of the contralateral and ipsilateral central pads. Conversely, in the anterior region of SII (the region that exhibited the largest response to contralateral stimulation), the response to bilateral stimulation was consistently smaller than (by approximately 30–35%) the response evoked from the contralateral central pad.
This report addresses the response of SI cortex to the same modes of stimulation used in the above-described study that focused on SII (i.e., contralateral, ipsilateral, and bilateral stimulation of the central pads of the forepaws). The central finding is that flutter stimulation of the ipsilateral central pad exerts a suppressive/inhibitory influence on the SI response to a 25 Hz flutter stimulus to the contralateral central pad (forepaw). In addition, the temporal relationship between stimulus-evoked activity in selected locations in the responding regions of SI and SII is evaluated quantitatively (using the approach of correlation mapping), revealing a previously unrecognized, and presumably functionally important high degree of coordination between the activities evoked by forepaw stimulation in both SI and the recently identified  anterior vs. posterior components that comprise SII cortex in the same hemisphere.
Comparisons between SI and SII responses
The findings of this study demonstrate that bilateral flutter stimulation of the central pads of the forepaws evokes an SI response significantly smaller than the response evoked when the stimulus is applied contralaterally. At the locus of the maximal OIS response evoked in the SI region by a contralateral stimulus, bilateral stimulation evoked a response that was, on average, 35% smaller than that evoked by the contralateral stimulus. Concurrently, at the locus of the maximal OIS response evoked by contralateral stimulation in anterior SII (reported in a previous study; ), bilateral stimulation evoked a response that was, on average, 35% lower than the activity evoked by a contralateral stimulus. The same conditions that led to the decrease in activity in SI and anterior SII also led to an increase in activity in posterior SII .
Although the neural mechanisms responsible for the above-described effect remains uncertain, some workers have reported that callosally-transmitted inputs exert modulatory, but inconsistent effects on SI neurons. Schnitzler et al , using MEG in humans, showed that tactile stimulation of one hand enhanced the response of ipsilateral primary somatosensory cortex (SI) to median nerve stimulation. Conversely, Korvenoja et al  reported that activation of SI (measured using MEG in humans) by electrical stimulation of the contralateral median nerve was suppressed during movement of the fingers of the ipsilateral hand. In addition, Hoechstetter et al.  described "interactions" in SII cortex (defined as a response that was less than a summation of the responses to independent ipsilateral and contralateral stimulation) during bilateral stimulation, but reported that the response in SI evoked by a contralateral stimulus was not altered by the addition of an ipsilateral stimulus. Shimojo et al  also found no difference in sources localized to SI evoked by unilateral versus bilateral stimulation. Most recently, Staines, et al,  reported data (fMRI) showing that SI activity evoked by passive bilateral stimulation is weaker than the SI activity evoked by passive unilateral stimulation. Other findings in the same report showed that the modulation of SI activity, particularly in the case of bilateral stimulation, was task-dependent. Others have shown that the activity evoked in SI by a unilateral stimulus can be modulated in a context-dependent manner, both in humans (e.g., [10, 11]) and in other primates (e.g., [12–15]).
Although an influence mediated via direct callosal projections from ipsilateral SI to contralateral SI  should not be ruled out, the data presented in this study lead us to propose that SII is the major source of the modulated SI response to contralateral skin stimulation that is observed under a variety of stimulus conditions [16–19]. Whereas the available literature is contradictory , it is clear that SII in cats receives its principal input from the thalamus [21–25]. While some investigators have proposed that monkey SII occupies a higher position in the somatosensory information processing hierarchy than does SII in cat , others have warned that "these are basically descriptive schemes of connections that do not illuminate what features of somesthesis are selectively projected" and that "they also tend to ignore potential interdependence between SI and SII" . The OIS observations in the present study obtained by simultaneously imaging the contralateral SI and SII in cats during ipsilateral stimulation of the central pad revealed that the time course of the optical response (increasing absorbance) evoked in posterior SII is negatively correlated with the time course of the optical signal in SI and anterior SII. Perhaps more significantly, the results obtained by correlation of the responses evoked under contralateral and bilateral stimulus conditions revealed a similar relationship between the cortical activity evoked in SI, anterior SII and posterior SII – in this case, the time course of the activities of SI and anterior SII are positively correlated under the bilateral stimulus condition, whereas under the same condition those activities are negatively or only weakly correlated with the activity in posterior SII. A plausible (but not necessarily the only) explanation for these outcomes is that the activity evoked in posterior SII exerts an inhibitory influence on SI via the extensive corticocortical connections known [27, 28] to link topographically corresponding regions in SI and SII.
An extensive literature addresses the neuroanatomical routes by which information about the status of skin mechanoreceptors accesses SI and SII (see [27, 28] for review). While the data presented in this paper neither extend or modify what is known about the routes by which information reaches SI and SII, they (along with the evidence presented in our previous paper – ) address the issue of whether, and to what extent, the responses of SI, anterior SII, and posterior SII in the same hemisphere are independent. The data presented here, in conjunction with evidence published previously , shows that nonnoxious mechanical skin stimulation evokes afferent activity that is conveyed via central somatosensory pathways to SII in both the contralateral and the ipsilateral hemispheres, and raises the possibility that unlike the activity evoked by contralateral flutter, the SII activity generated by ipsilateral skin stimulation may depress (perhaps via inhibitory processes mediated by corticocortical connections) the response of SI to ongoing skin stimulation. Previously, we postulated that SII activity levels modulated the SI response when the SII activity was evoked by vibratory stimuli . That study showed that contralateral vibration increased SII activity levels which were correlated with decreases in SI vibration-evoked activity. The findings make it seem likely that, at least in cat, the degree to which SII activation modifies the SI response to skin stimulation depends on the attributes of the peripheral stimulus – that is, that SI activity is modified by SII activity in a stimulus-dependent manner.
The responses evoked by contralateral, ipsilateral and bilateral flutter stimulation of the central pad of the cat forepaw indicate that the response of SI evoked by contralateral stimulation is reduced in the presence of an ipsilateral stimulus. Correlation analysis of the responses evoked by ipsilateral skin flutter stimulation showed that activity in posterior SII (the region of SII that maximally responds to an ipsilateral stimulus) is negatively correlated with the activity in SI. Additionally, correlation mapping of the results obtained from the contralateral vs. bilateral stimulus conditions demonstrated that the time course of the activities evoked in SI and anterior SII by these conditions are similar. The data lead to the proposal that increasing levels of activity in posterior SII evoked by an ipsilateral skin stimulus suppress/inhibit the responses normally evoked in both anterior SII and SI by contralateral stimulation.
Subjects & preparation
Adult cats (males and females; n = 5) were subjects. All surgical procedures were carried out under deep general anesthesia (1 – 4% halothane in a 50/50 mixture of oxygen and nitrous oxide). After induction of general anesthesia the trachea was intubated with a soft tube and a polyethylene cannula was inserted in the femoral vein to allow administration of drugs and fluids (5% dextrose and 0.9% NaCl). For each subject, a 1.5 cm diameter opening was made in the skull overlying somatosensory cortex, a chamber was mounted to the skull over the opening with dental acrylic, and the dura overlying anterior parietal cortex was incised and removed. Following the completion of the surgical procedures all wound margins were infiltrated with long-lasting local anesthetic, the skin and muscle incisions were closed with sutures, and each surgical site outside the recording chamber was covered with a bandage held in place by adhesive tape.
Subjects were immobilized with Norcuron and ventilated with a gas mixture (a 50/50 mix of oxygen and nitrous oxide; supplemented with 0.1 – 1.0% halothane when necessary) delivered via a positive pressure respirator 1–3 hours prior to the data acquisition phase of the OIS imaging experiments. Respirator rate and volume were adjusted to maintain end-tidal CO2 between 3.0 – 4.0%; EEG and autonomic signs (slow wave content; heart rate, etc.) were monitored and titrated (by adjustments in the anesthetic gas mixture) to maintain levels consistent with light general anesthesia. Rectal temperature was maintained (using a heating pad) at 37.5°C.
Euthanasia was achieved by intravenous injection of pentobarbital (45 mg/kg) and by intracardial perfusion with saline followed by fixative (10% formalin). Following perfusion fiducial marks were placed to guide removal, blocking, and subsequent histological sectioning of the cortical region studied. All procedures were reviewed and approved in advance by an institutional committee and are in full compliance with current NIH policy on animal welfare.
Stimuli and stimulus protocols
Results were obtained during stimulation of the contralateral central pad of the forepaw and/or the ipsilateral central pad of the forepaw. The stimuli always consisted of sinusoidal vertical skin displacements (25 Hz, 400 microns, stimulus duration 5 sec, inter-stimulus interval 60 sec) and were applied using a pair of servocontrolled transducers (Cantek Enterprises, Canonsburg, PA) that is capable of delivering sinusoidal stimuli in the range of 1–250 Hz at amplitudes in the range of 0–1000 microns. The stimuli were delivered independently to the ipsilateral and contralateral skin sites, and also were applied simultaneously to both sites (bilateral stimulation). The stimulus probes were positioned 500 microns beyond the point at which skin contact was detected (via force transducer on the Cantek). The bilateral stimulus protocols reported in this paper were synchronized to start and stop at the same time. The contralateral, ipsilateral and bilateral stimuli were interleaved on a trial-by-trial basis. This approach was used to control for temporal changes in cortical "state" unrelated to stimulus conditions which, if unrecognized, might obscure or modify any differences between the optical responses evoked by the contralateral, ipsilateral and bilateral stimulus conditions.
Near-infrared (IR; 833 nm) OIS imaging was carried out using an oil-filled chamber capped with an optical window  Images of the exposed cortical surface were acquired 200 msec before stimulus onset ("reference" or "prestimulus" images) and continuously thereafter ("poststimulus" images; at a resolution of one image every 0.5 to 1.5 sec) for 15–20 sec following stimulus onset. Exposure time was 200 msec. Absorbance images were generated by subtracting each prestimulus (reference) image from its corresponding poststimulus image and subsequently dividing by the reference image. Averaged absorbance images typically show regions of both increased absorption of IR light and decreased absorption of light (to a depth of approximately 1400 microns) which have been shown to be accompanied by increases and decreases in neuronal activation, respectively [30–35].
Correlation maps were constructed for comparison of spatio-temporal characteristics of the OIS response. One aspect of this method of analysis has been previously described in detail [18, 29]. Briefly, the correlation maps in Figure 6 were constructed by choosing a reference region within the imaged field and computing the intensity correlation rij between the absorbance value of each pixel (i, j) and the average absorbance value within the reference region over the time from stimulus onset to stimulus offset. The region selected as the reference was defined by a boxel (π mm2 area) centered on the region of interest (ROI). Each pixel (i, j) on the correlation map is represented by a coefficient of determination r2 ij (-1 <r2 < 1; - 1 indicates negative correlation; + 1 indicates positive. The statistical significance of each of the correlations was tested with the standard t-test. A second type of correlation map, or cross-correlation map, was generated in a similar manner (such as that computed in Figure 7). In this method, rather than correlating each pixel with the time course observed at one particular cortical region for the same stimulus condition, cross correlation was performed between the time courses of absorbance values obtained at the same spatial location (i, j) for different stimulus conditions. Thus, each coefficient of determination r2 ij represents how similar (positive correlation) or how different (negative correlation) the response in a region is to a change in stimulus condition.
Histological procedures/identification of cytoarchitectural boundaries
At the conclusion of the experiment, the imaged cortical region was removed immediately following intracardial perfusion with saline and fixative. The region then was blocked, postfixed, cryoprotected, frozen, sectioned serially at 30 μm, and the sections stained with cresyl fast violet. The boundaries between adjacent cytoarchitectonic areas were identified by scanning individual sagittal sections separated by no more than 300 mm and were plotted at high resolution using a microscope with a drawing tube attachment. The resulting plots then were used to reconstruct a two-dimensional surface map of the cytoarchitectonic boundaries within the region studied with optical and neurophysiological recording methods. The locations of microelectrode tracks and electrolytic lesions evident in the histological sections were projected radially to the pial surface and transferred to the map of cytoarchitectonic boundaries reconstructed from the same sections. As the final step, the cytoarchitectonic boundaries (along with the locations of microelectrode tracks and lesions whenever present) identified in each brain were mapped onto the images of the stimulus-evoked intrinsic signal obtained from the same subject, using fiducial points (made by postmortem applications of india ink or needle stabs) as well as morphological landmarks (e.g., blood vessels and sulci evident both in the optical images and in histological sections). Locations of cytoarchitectonic boundaries were identified using established criteria [36–38].
This work was supported, in part, by NIH NS050587 (M. Tommerdahl, P.I.) and NIH NS35222 (B. Whitsel, P.I.).
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