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1Department of Psychology, University of Colorado at Boulder, Boulder, Colorado; and 2Department of Veterinary Comparative Anatomy, Pharmacology and Physiology, Washington State University, Pullman, Washington
Submitted 28 June 2006; accepted in final form 25 September 2006
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ABSTRACT |
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INTRODUCTION |
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; Johnson 1990). The anatomy of primary somatosensory cortex in the rat (SI) was previously well characterized and forms a single somatotopically organized representation of the body with the hindquarters pointed medially, the limbs rostrally, and the facial representation dominated by the more lateral and extensive posteromedial barrel subfield (PMBSF; Chapin and Lin 1990). In contrast to primary somatosensory cortex, the number and somatotopic organization of secondary somatosensory zones (SII) is less clear.
Early recordings of somatosensory evoked field potentials, mapped from the cortical surface, identified a single somatotopic organization of SII, lateral to SI, suggesting an image of the body that was upside down and pointed rostrally (Woolsey 1952; Woolsey and LeMessurier 1948). Although these results were initially confirmed with microelectrode unit recording (Welker and Sinha 1972), subsequent microelectrode and histological studies suggested that lateral SII was actually composed of two complete somatotopic maps (Fabri and Burton 1991; Li et al. 1990; Remple et al. 2003). The first (SII) was of upright orientation and the second [parietal ventral area (PV)] was positioned more laterally and formed a mirror image of SII [with the exception of Carvell and Simons (1986) who found a single body representation in SII that was upright]. Similar dual representations of SII and PV were proposed for some marsupials and many placental mammals, including man (Disbrow et al. 2000).
Even though recent microelectrode unit recording (Remple et al. 2003) and anatomical tract tracing studies (Fabri and Burton 1991; Li et al. 1990) provide compelling evidence for the existence of at least two secondary regions of somatosensory cortex in the rat, because of the limited spatial sampling of these methods, the exact location, orientation, somatotopic organization, and cortical magnification of somatic representations within these regions remain the focus of some debate. For this reason, we developed methods for mapping evoked field potentials from the cortical surface with high spatial resolution electrode arrays, permitting simultaneous sampling from a broad reach of cortex and comparison of the relative locations and amplitudes of secondary cortical responses during somatosensory stimulation. This work indicated a single secondary vibrissa representation but two representations of the body, positioned rostrolateral and caudomedial to auditory cortex (Brett-Green et al. 2004). However, these studies were also limited by sampling from only a 3.5-mm2 area of cortex in a single-array placement. The need for repositioning made it impossible to accurately determine the relative positions of somatotopic representations, both between the two secondary zones and in relation to corresponding representations in SI. Multiple-array placements also precluded estimates of the relative amplitude of responses between regions that could indicate differential cortical magnification within the somatotopic map. Although representing an improvement over the spatial sampling of single-electrode–unit recording, the use of small surface electrode arrays still introduced the possibility of missing active regions and, equally important, failing to rule out inactive or at least minimally active regions of secondary somatosensory cortex.
To overcome these limitations in the present study, we reexamined secondary and primary somatosensory cortex of the rat using a 256-electrode array and data-acquisition system that permitted simultaneous recording from nearly the entire cerebral hemisphere in a single placement. We also improved the spatial accuracy of resulting localizations by devising a method of coordinate transformation to adjust for slight changes in the location and orientation of the electrode array between animals. Finally, we applied statistical analysis to determine the significance and reliability of somatotopic representations derived from epipial field potential mapping, a procedure made possible by simultaneous sampling of responses from multiple cortical regions.
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METHODS |
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All procedures were conducted within the guidelines established by the University of Colorado Institutional Animal Care and Use Committee. Adult male Sprague–Dawley rats (n = 11, 350–365 g) were anesthetized to surgical levels using subcutaneous injections of ketamine (71 mg/kg of body weight), xylazine (14 mg/kg), and acepromazine (2.4 mg/kg). Animals were placed on a regulated heating pad to maintain normal body temperature (37°C). Anesthesia levels were maintained throughout the experiment so that the corneal and flexor withdrawal reflexes could barely be elicited. A unilateral craniotomy was performed over the right hemisphere extending from bregma to 3 mm rostral of lambda and from the midsagittal suture past the lateral aspect of the temporal bone, exposing a maximal area of the surgically accessible hemisphere. The dura was reflected and the exposed cortex regularly doused with Ringer solution containing (in mM): NaCl 135; KCl 3; MgCl 2; and CaCl 2 (pH 7.4 at 37°C). At the conclusion of the experiment, animals were killed by anesthesia overdose without ever regaining consciousness.
Stimulation
Vibrissae on the left mystacial pad were trimmed to 2 cm and displaced about 300 µm (duration: 0.1 ms; interstimulus interval: 1 s) by inserting them into the ends of 6-cm stainless steel hypodermic tubes attached to laboratory-built solenoids (Barth 2003; Jones and Barth 1999). Somatic stimulation was achieved in two ways. In most animals, electrical stimulation was used. The hindpaw (HP), hindlimb (HL), midtrunk (MT), forepaw (FP), forelimb (FL), cheek (CH), ventral and dorsal eye areas (EV and ED, respectively), and pinna (PN) were shaved and lightly coated with conductive jelly. A bipolar electrode (500-µm tips; 1-mm separation) attached to a constant-current source delivered biphasic current pulses (1 ms; 0.1–2 mA) to the exposed skin. Alternatively, in several animals mechanical stimulation was delivered in separate trials to the same body parts (except PN) using a blunt stainless steel wire (diameter: 0.5 mm; length: 2 cm) attached to a balsa wood stick (diameter: 5 mm; length: 15 cm) that was driven perpendicularly into the skin (about 0.5–1 mm; 1-ms pulses) by a silent solenoid. Mechanical stimulation of the vibrissae and skin was inaudible, but was nonetheless checked for auditory artifacts by repeating trials with the stimulators in the same location but adjusted for no contact. Except during auditory stimulation, the ears were bilaterally occluded with soft earplugs inserted in the external auditory meatus. Auditory click stimuli (0.1-ms monophasic pulses) were delivered using a high-frequency piezoelectric speaker placed about 15 cm lateral to the contralateral ear. Visual stimulation (15-ms pulses) was delivered with an array of five high-intensity light-emitting diodes (white) positioned about 2 cm from the contralateral eye. During auditory, somatosensory, and visual stimulation, intensities were adjusted to the lowest level yielding a stable evoked potential.
Evoked potential recording
Epipial maps of somatosensory, auditory, and visual evoked potentials (SEPs, AEPs, and VEPs, respectively) were recorded using a flat multielectrode array consisting of 256 silver wires in a 16 x 16 grid (tip diameter: about 100 µm; interelectrode spacing: 500 µm) covering a 7.5 x 7.5-mm area of the right hemisphere in a single placement. The array was pressed against the cortex with sufficient force to establish contact of all electrodes. The required pressure had no effect on evoked potential amplitude, poststimulus latency, or morphology when compared with potentials recorded previously with more lightly placed small arrays. Recordings were referenced to a Ag/AgCl ball electrode secured over the contralateral frontal bone and were simultaneously amplified (x2,000; NerveAmp, Center for Neural Recording, Washington State University, Pullman, WA), analog filtered (band-pass cutoff = –6 dB at 0.1 to 3,000 Hz, roll-off = 5 dB/octave) and digitized at 10 kHz. Evoked potentials were averaged over 120 stimulus presentations.
Data collection and analysis
Regions of primary and secondary sensory cortex were estimated from interpolated (bicubic spline) maps of evoked potential amplitude across the recording array at select poststimulus latencies. The initial positive component (P1) of the evoked potential complex occurred at the shortest poststimulus latency in primary sensory cortex and the center of its mapped amplitude peak was visually identified and used to locate cortical representations in this region (an example of the primary response to stimulation of vibrissa E3 is shown in Fig. 1C, left map). The P1 in secondary cortex occurred significantly later (latencies were evaluated with Student's t-test with significance set to P 
0.05) and was spatially separate from primary responses (Fig. 1C, right map). Although the number of stimulated vibrissae differed in several animals, in all animals, primary and secondary responses from all body parts and vibrissae C1, C4, E3, and A3 were recorded (in six animals, responses from all 25 macrovibrissae were also recorded). To adjust for slight variability of the location and orientation of the recording array across animals, the primary and secondary representations for these four vibrissae and nine body parts in each animal were compared with the mean loci averaged across animals. The loci of all responses for a given animal were then iteratively shifted and rotated as a group to achieve a best fit to the mean using a simplex algorithm (Press et al. 1986) to minimize the squared error. Differences between aligned cortical representations were evaluated using a Fisher's least significant difference (LSD) procedure (Snedecor and Cochran 1980). This involved first performing a one-way ANOVA to test whether all group means were equal. Significant F-ratios were then followed by post hoc Student's t-test to evaluate significant differences between the mean loci of pairs of body part representations. Significance for both the F and t statistics were set to P 0.05. Variability was reported as the SE.
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RESULTS |
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0.05). This temporal and spatial separation permitted computation of separate topographical maps for primary (Fig. 1C, left map) and secondary (Fig. 1C, right map) cortex that were then used to log the coordinates of these two areas by visually identifying their amplitude maxima (Fig. 1C, white crosses). This method was used to locate the primary and secondary representations of both vibrissa and nonvibrissa body parts. Responses in auditory (Fig. 1D, left map) and visual (Fig. 1D, right map) cortex were also recorded using auditory clicks and light flashes, respectively. Resulting maps of each area were averaged across animals and the 50% isopotential contours outlined (Fig. 1D, dashed lines) for use as anatomical landmarks of auditory and visual cortex for subsequent illustration. No attempt was made to separate primary and secondary cortex in these modalities.
Maps of the early latency P1 evoked by stimulation of each of the 25 major vibrissae were averaged across animals (n = 6), resulting in a grand average map reflecting the location and extent of the PMBSF in primary somatosensory cortex (Fig. 2A, white box). Locations of each vibrissa representation within this field, computed from the single vibrissa responses, were stable across animals (average SE: ±82.8 µm) and significantly separable (P < 0.01). They conformed to the established organization of this region, with a rostrocaudal pattern of arcs but inverted pattern of rows (i.e., the ventral E row is represented dorsally). A similarly computed grand average map of longer-latency responses in secondary vibrissa cortex indicated an elongated region lateral to the PMBSF, canted along the rostrolateral axis, and abutting auditory cortex caudally (Fig. 2C, white box). The pattern of individual vibrissa representations within this region was quite orderly (Fig. 2D), indicating a rostrocaudal arrangement of the arcs like that of the PMBSF, but an upright organization of the rows. Successive rows were staggered on the rostrocaudal axis, resulting in an elongation of the somatotopic map that mirrored that of the PMBSF. The locations of individual vibrissa representations, even in this small area, were sufficiently stable (average SE: ±81.9 µm) across animals to be significantly separable (P 0.05), except for vibrissa pairs a3–b3, a4–b4, b2–b3, c3–d1, e1–d2, e1–d3, e1–d4, e1–e2, and e2–e3. Using the locus of the C1 whisker representation in primary cortex as a reference point, the representation of the same whisker in secondary vibrissa cortex was positioned 0.54 ± 0.1 mm rostrally and 2.27 ± 0.08 mm laterally. The entire secondary representation for all 25 vibrissae extended 2.09 ± 0.09 and 1.09 ± 0.05 mm on the rostrocaudal and dorsoventral axes, respectively.
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; Krubitzer et al. 1986; Remple et al. 2003). A notable distinction between SII and PV was the lack of facial (except for the pinna) and vibrissal representation in PV. This distinction was also clear in the relative amplitude of long-latency responses in these regions. Selective grand average maps representing the nonvibrissa facial regions (PN, ED, EV, and CH; Fig. 5A, left map; arrow) versus the limbs (HL, HP, FL, and FP; Fig. 5A, right map; arrow) highlight the preferential sensitivities of SII and PV, respectively. The largest peak-to-peak (P1 to N1) responses in PV resulted from stimulation of the hindpaw and forepaw, followed closely in amplitude by the hindlimb and forelimb (Fig. 5B, blue bars). These same body parts yielded the smallest responses in SII (Fig. 5B, red bars) and significantly smaller than their corresponding amplitudes in PV. The midtrunk was the only body part to be equally represented in both PV and SII and did not significantly differ between the two regions. The pinna produced the largest amplitude secondary response recorded in this study and dominated SII with only a weak representation in PV. The dorsal and ventral eyes, cheek, and vibrissae (averaged across C1, C4, A3, and E3; n = 11) also yielded large responses in SII with no detectable PV response in any of the animals.
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DISCUSSION |
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; Fabri and Burton 1991; Hoffer et al. 2003) and electrophysiological unit (Carvell and Simons 1986; Remple et al. 2003) studies in the mouse and rat and earlier SEP mapping studies in the rat (Barth et al. 1993; Brett-Green et al. 2000, 2004; Di et al. 1994; Menzel and Barth 2005), we found a large secondary vibrissa representation just lateral to the PMBSF. The present data indicate that the vibrissa representation is upright and rostrally pointed with rows staggered on the rostrocaudal axis. Also, similar to a recent SEP mapping study of rat parietotemporal cortex (Brett-Green et al. 2004), we found two distinct secondary representations of the body, one caudomedial and the other rostrolateral to auditory cortex. The present results provide evidence that the caudal secondary body representation is upright and continuous with that of the vibrissa. We therefore regard this as a single somatotopic map, dominated by representation of the face, constituting area SII. A second smaller and inverted somatotopic map, dominated by representation of the distal extremities, is located in the far lateral temporal cortex and identified as area PV.
Primary somatosensory representations of the vibrissae and soma, derived here from epipial field potential maps, form an inverted rattunculus with caudally pointed limbs that corresponds closely to both anatomical and functional studies of this area (for a review, see Chapin and Lin 1990). This region was mapped to provide a template of SI for comparison to the secondary sensory regions. However, these data also provide an indication of the accuracy of our methods when used to chart a cortical region with well-established somatotopy. The average SE of localization in the PMBSF and somatic SI was ±82.8 and 84.3 µm, respectively. This is well below the 500-µm interelectrode spacing of the recording array. Two factors contribute to this localization accuracy. First, the locations of amplitude peaks in epipial maps are derived from two-dimensional bicubic spline interpolations of responses from multiple electrodes. Thus spatial gradients of the response improve localization accuracy in a way similar to the simple procedure of triangulating on a single location from several widely spaced sensors. However, the variability of localization within the barrel field reported here is still less than half that reported in a recent study using similar mapping methods (±190 µm; Rodgers et al. 2006). Much of this improvement is explained by the additional use of coordinate translation and rotation of each animal's grouped loci to fit those averaged across animals (see METHODS), providing a compensation for slight differences in array location and orientation across animals. Indeed, when the variability of localizations within the barrel field in the present study was recomputed without this adjustment, it increased to an average SE of ±223 µm.
This accuracy permitted us to establish a detailed map of the somatotopic organization of secondary vibrissa cortex. Early evoked potential studies in a number of species suggested the existence of a secondary trigeminal representation positioned just lateral to the face region of primary somatosensory cortex (Benjamin and Welker 1957; Bromiley et al. 1956; Lende and Woolsey 1956; Woolsey 1958). More recent anatomical work in the rat using anterograde and retrograde tracing of PMBSF projections (Hoffer et al. 2003; Koralek et al. 1990) revealed a topographically organized vibrissa representation of SII that is just lateral to and mirroring the PMBSF, similar to earlier unit mapping studies of the mouse (Carvell and Simons 1986). The location, orientation, and spatial extent of their vibrissa SII is in accord with the present data.
However, there are several notable differences between our results and previous reports. First, we were able to establish the somatotopy of all 25 macrovibrissae, revealing a highly organized pattern in which the rows are staggered rostrally along the mediolateral axis. Thus the representations of the most dorsal rows (A and B) extend far more caudally than previously appreciated and occupy much of the region between the PMBSF and auditory cortex, with the rostrocaudal extent of vibrissa SII alone approaching 2 mm. Second, tracing studies indicated substantial overlap of labeling within vibrissa SII, particularly with dual injections within the same row of the PMBSF (Hoffer et al. 2003; Koralek et al. 1990). Divergent projections from SI to SII were also thought to result in multivibrissa responsiveness in SII compared with SI of the mouse (Carvell and Simons 1986), possibly reflecting a propensity for intrarow integration in SII that exceeds that of the PMBSF (Carvell and Simons 1986; Hoffer et al. 2003). Yet, our data suggest that, despite this propensity, vibrissa SII maintains a remarkable degree of functional segregation within and between the rows and arcs. This is reflected both in the orderly somatotopic organization recorded here and in the fact that all but a few of the single vibrissa loci were significantly separable. Third, both anatomical (Fabri and Burton 1991; Hoffer et al. 2003) and electrophysiological (Remple et al. 2003) studies suggested a second inverted representation of the vibrissae in the far lateral region of PV. We recorded no vibrissa responses from this lateral area. One possible explanation for this discrepancy is that we failed to record sufficiently lateral to detect this representation. However, our electrodes extended to the perirhinal cortex (and in a few instances the rhinal fissure), exceeding the reported lateral extent of PV, which is separated from the rhinal fissure by perirhinal cortex (PR; Fabri and Burton 1991). A more likely explanation is that these projections are sparse and thus exert only a weak influence on the epipial evoked potential. This conclusion is supported by the preferential responsiveness of PV to stimulation of the limbs, particularly the distal extremities. The only facial area yielding recordable responses in PV is the pinna and, even here, the relative amplitude of the responses is roughly sevenfold greater in SII.
A final difference between our results and previous work is that we found a consistent and significant increase in poststimulus latencies of the P1 peak in SII compared with SI and a further latency increase in PV compared with SII. In contrast, recent unit studies found no latency differences in SI compared with SII neurons (Kwegyir-Afful and Keller 2004). This may be attributable to methodological differences. Whereas Kwegyir-Afful and Keller (2004) compared response latencies of SI barrel (layer IV) neurons and SII (layers II and VI) neurons, the P1 recorded in epipial field potential measurements reflects postsynaptic potentials dominated by pyramidal cells in the supragranular layers (Di et al. 1990). The central tendency of supragranular P1 responses shifts toward longer latencies in SII and PV, possibly reflecting multisynaptic connections between SI and secondary cortex and/or temporal differences in thalamocortical relay to primary and secondary zones.
The largest amplitude responses in secondary somatosensory cortex are evoked by stimulation of facial regions and form a continuation of the secondary vibrissa map. Stimulation of the cheek at a location midway between the caudal vibrissae and the ventral eye evokes responses just caudal to and partially overlapping those of caudal vibrissa SII, also in the region separating the PMBSF and auditory cortex. Other facial representations follow an orderly progression caudally (ventral and dorsal eye) and laterally (pinna). The midtrunk is also strongly represented more laterally with weaker representations of the limbs that, as a group, form an inverted image of SI somatotopy. The fact that somatic and vibrissa responses in cortex just lateral to SI form a continuous trigeminal and spinal representation that is upright, rostrally oriented, and mirrors SI leads us to the conclusion that this is a single region. We have correspondingly labeled the area "SII" to distinguish it from the more lateral and rostral "PV" according to the nomenclature of Krubitzer et al. (1986).
Indeed, our description of SII most closely resembles that noted by Krubitzer et al. (1986) in microelectrode studies of the gray squirrel, where the body and face representation was described as upright and rostrally pointed, with the head represented along the lateral SI border and the body medial and slightly caudal to auditory cortex. Although our results are also similar to previous descriptions of SII derived from microelectrode (Remple et al. 2003) and anatomical (Fabri and Burton 1991) studies in the rat, there is an important distinction. In these studies, the upright body representation of SII was located rostral to auditory cortex, with representation of distal extremities contiguous with an inverted representation in PV. We found little responsiveness to somatic stimulation in the region between vibrissa SII and PV. There are several possible explanations for this distinction. Remple et al. (2003) performed all recordings rostral to auditory cortex, possibly missing large responses from the caudally extending face representation of SII recorded here. With tracer injections in the trunk or distal limb, Fabri and Burton (1991) reported inconsistent labeling of cells in a posterolateral area (PL), similar in location to our somatic SII. Unfortunately, their injection sites did not include SI representations of facial regions aside from the vibrissae, where we obtained the largest responses in caudal SII. Thus they may not have appreciated the contributions of more caudal facial regions to the SII somatotopic map. It is possible that, similar to our failure to record vibrissa responses from PV because of their weak representation, we also failed to record somatic responses just beneath vibrissa SII reported by others. However, we did record somatic responses from this area, although they were concentrated along the rostral secondary belt region of auditory cortex and formed a multisensory zone with a somatotopy that does not closely resemble that of somatic SII from other studies (Menzel and Barth 2005). Multisensory cortex may have contributed to somatic responsiveness and labeling in these studies as well, a possibility worthy of consideration in future investigations. In light of the large-amplitude facial responses that smoothly continue, and are of the same upright orientation as those in vibrissa SII, and the contiguous somatic representation of an upright body posterior and medial to auditory cortex, we combine this entire somatotopic map as a single and quite extensive representation of SII.
By comparison, our map of PV is quite small. Similar to previous studies in the rat (Fabri and Burton 1991; Remple et al. 2003) and squirrel (Krubitzer et al. 1986), our results indicate an inverted and rostrally oriented body representation within PV in a location lateral to the upright SII. As noted earlier, we did not also record contiguous vibrissa responses in this representation. The missing vibrissa portion of our PV somatotopic map also differs substantially from that proposed for the gray squirrel (Krubitzer et al. 1986), which includes an upright vibrissa representation abutting SI laterally and just rostral to the vibrissa representation in SII. This may represent a significant difference between PV in the squirrel and the rat or, alternatively, it is possible that the vibrissa representation noted in the squirrel was actually a rostral extension of vibrissa SII. Without extensive mapping performed here, the rostrally staggered configuration of vibrissa rows could lead to the conclusion that there might be two separate representations when there is only one.
Although there has been some dispute concerning the number and organization of secondary somatosensory areas in rats (Koralek et al. 1990; Li et al. 1990), the weight of evidence is for at least two complete and topographically organized representations of the body surface, with SII just lateral to SI (Brett-Green et al. 2004; Fabri and Burton 1991; Koralek et al. 1990; Li et al. 1990; Remple et al. 2003; Welker and Sinha 1972) and PV positioned further lateral, approaching the rhinal fissure (Brett-Green et al. 2004; Fabri and Burton 1991; Li et al. 1990; Remple et al. 2003; Welker and Sinha 1972). The present results confirm the existence of a separate SII and PV in the rat and extend these findings by providing a detailed somatotopy of both regions. Unlike anatomical tracing studies and single-unit electrophysiology, high-resolution field potential mapping performed here also yields an estimate of the relative cortical magnification of representations within each area. What emerges is an SII dominated by the vibrissae and face and a PV dominated by the distal extremities. If size may be related to relative importance, then SII is by far the most important area of secondary somatosensory cortex, occupying a total area spanning about 1 x 5 mm of parietal cortex, almost a quarter the size of SI and fivefold the size of PV. Given the relative importance of the vibrissae and face to the rat for exploring the environment, it is not surprising that these representations dominate the somatotopy of both SI and SII. Even though the function of secondary cortex is poorly understood (Burton 1986), the large size and detailed somatotopy of SII suggest a processing role that parallels that of SI. Hemispheric mapping of SI, SII, and PV provides a means of rapidly and accurately determining the locus and extent of these regions for future tracing, lesion, and behavioral studies, shedding further light on their relative contribution to somatosensory information processing.
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GRANTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: D. S. Barth, Department of Psychology, University of Colorado, Campus Box 345, Boulder, Colorado 80309-0345 (E-mail: dbarth{at}psych.colorado.edu)
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K. M. Rodgers, A. M. Benison, A. Klein, and D. S. Barth Auditory, Somatosensory, and Multisensory Insular Cortex in the Rat Cereb Cortex, December 1, 2008; 18(12): 2941 - 2951. [Abstract] [Full Text] [PDF]
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B. de Celis Alonso, A. S. Lowe, J. P. Dear, K. C. Lee, S. C. R. Williams, and G. T. Finnerty Sensory Inputs from Whisking Movements Modify Cortical Whisker Maps Visualized with Functional Magnetic Resonance Imaging Cereb Cortex, June 1, 2008; 18(6): 1314 - 1325. [Abstract] [Full Text] [PDF]
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 N. J. G. Maandag, D. Coman, B. G. Sanganahalli, P. Herman, A. J. Smith, H. Blumenfeld, R. G. Shulman, and F. Hyder Energetics of neuronal signaling and fMRI activity PNAS, December 18, 2007; 104(51): 20546 - 20551. [Abstract] [Full Text] [PDF]
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