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Department of Psychology, University of Colorado at Boulder, Boulder, Colorado 80309
Submitted 16 September 2003; accepted in final form 27 October 2003
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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; Hall and Lindholm 1974; Koralek et al. 1990; Wallace 1987; Welker 1971, 1976; Woolsey and LeMessurier 1948), mouse (Angel and Lemon 1975; Wallace 1987; Woolsey 1967), and squirrel (Krubitzer et al. 1986). However, the number and somatotopic organization of secondary somatosensory regions (SII) is still the subject of some debate.
A single area of SII in the rat (Akers and Killackey 1978; Chapin and Lin 1984; Fabri and Burton 1991; Koralek et al. 1990; Wallace 1987; Welker and Sinha 1972; Woolsey and LeMessurier 1948) and mouse (Carvell and Simons 1986, 1987; Wallace 1987; Woolsey 1967) has been identified lateral to SI, just rostral to auditory cortex. Somatotopic maps using evoked potential (Woolsey 1952; Woolsey and LeMessurier 1948) and microelectrode unit recordings (Welker and Sinha 1972) suggest an image of the rat's body in this region that is upside down and oriented rostrally. However, more recent examination of ipsilateral cortical connections of SI (Fabri and Burton 1991) indicate somatotopically organized reciprocal connections between SI and two mirror image areas of secondary cortex in the lateral region: one overlapping classically defined SII with the same somatotopic organization as previously reported and a second inverted image located more laterally near the rhinal fissure. Further complicating the issue of the number of secondary somatosensory areas in the rat are tracing studies that suggest that, in addition to a lateral SII, there may also be a second separate area of SII reciprocally connected with SI but positioned in a more caudal and medial locus (Fabri and Burton 1991; Koralek et al. 1990), similar to separate rostral and caudal secondary somatosensory zones identified in the squirrel (Krubitzer et al. 1986).
Even less well understood is the function of SII compared with SI. Recent studies in the rodent, combining somatosensory with either auditory (Brett-Green et al. 2003; Carvell and Simons 1986, 1987; Di et al. 1994; Ramachandran et al. 1993; Wallace et al. 2004) or visual stimulation (Barth et al. 1995; Ramachandran et al. 1993; Wallace et al. 2004), have suggested that one of the functions of SII, and indeed of secondary sensory cortex in general, may be in multisensory integration. However, while cells within SII responding to multisensory stimuli have been reported, the relative topographies of multisensory zones and SII have not been investigated in detail.
In this study, we used high-resolution epipial-evoked potential mapping to determine if rat SII is composed of one or more spatially discrete regions and to estimate its somatotopic organization. Although field potential mapping has a lower spatial resolution than microelectrode recording, it has the advantage that wide areas of cortex can be recorded simultaneously and it eliminates spatial sampling errors inherent in single microelectrode recording. In addition, field potential maps can identify and separate distinct cortical regions based on spatio-temporal differences in the evoked response complex (Barth and Di 1991; Barth et al. 1993; Di and Barth 1991). We then compared maps of SII to regions where somatosensory and auditory responses overlap and interact to examine the involvement of secondary cortex in multisensory processing.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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All procedures were performed in accordance with University of Colorado Institutional Animal Care and Use Committee guidelines for the humane use of laboratory animals in biological research. Ten adult male Sprague-Dawley rats (300-400 g) were anesthetized to surgical levels using intramuscular injections of ketamine (71 mg/kg body weight), xylazine (14 mg/kg), and acepromazine (2.4 mg/kg), placed on a regulated heating pad, and maintained with subsequent injections throughout the experiment so that the eye blink reflex could be barely elicited. A unilateral craniectomy was performed over the right hemisphere, extending from bregma to lambda and from the midsagittal sinus lateral to the temporal bone, exposing a wide region of parieto-temporal cortex where the dura was reflected. Animals were killed by anesthesia overdose without regaining consciousness at the conclusion of the experiment.
Stimulation
Auditory click stimuli were delivered with a high-frequency piezoelectric speaker aligned with, and approximately 10 cm from, the contralateral ear. The ipsilateral ear was blocked with soft wax. Clicks were computer-controlled monophasic square-wave pulses (0.3 ms; 
50 db SPL at 10 cm). Silent stimulation of individual vibrissae on the contralateral mystacial pad was achieved with a pulsed (0.5 ms) electromagnet. Vibrissae were attached to a short ferrous wire about 10 mm from the mystacial pad. The wire was positioned 1.0 mm below the magnet. and pulsed (1 ms) stimulation displaced the vibrissae vertically by 0.5 mm. Silent electrical stimulation of discrete body regions was achieved with a bipolar stainless steel electrode (0.5 mm separation; 1-mm exposed tip) attached to a constant current source, delivering current pulses (1 ms) of minimum current (0.2-0.5 mA) required to produce a reliable evoked response with no noticeable muscle contractions when applied to the shaved skin pretreated with conductive jelly.
Data collection and analysis
Epipial maps of auditory and somatosensory evoked potentials (AEPs and SEPs, respectively) were recorded using a flat multielectrode array consisting of 64 silver wires in an 8 x 8 grid (tip diameter: 100 µm; inter-electrode spacing: 500 µm) covering a 3.5 x 3.5 mm area. Recordings were referred to a silver ball electrode secured over the contralateral frontal bone and were simultaneously amplified (10,000 times), analog filtered (band-pass cut-off = -6 dB at 0.001-3.000 Hz, roll-off = 5 dB/octave). and digitized at 10 kHz. Trials of separately evoked AEPs or SEPs consisted of a 25-ms baseline followed by 75 ms of poststimulus activity, averaged over 50-100 presentations. Evoked responses in Figs. 1, 2, 3, 4 reflect grand averages across six animals. Trials to examine multisensory interaction consisted of an initial auditory stimulus followed at 50 ms by a somatosensory stimulus. While simultaneous presentation of auditory and somatosensory stimuli were used to test multisensory interaction in our previous studies (Barth et al. 1995; Brett-Green et al. 2003; Di et al. 1994), the small amplitude SEPs evoked in SII by electrical stimulation of the skin in this study led us to use asynchronous presentation, because this was found to produce the strongest and most reliable interaction effects due to depression affected by inhibition following the response to the first excitatory stimulus. Multisensory potentials were averaged over 50-100 auditory, somatosensory, and auditory/somatosensory stimulations, randomized in their presentation sequence with an interstimulus interval of 1 s. Evoked responses in Figs. 5, 6, 7 reflect grand averages across the additional four animals used in the multisensory phase of the experiment. Single vibrissa-evoked SEPs were used to consistently align the array across animals, which, in previous studies, has been found to have a placement error of less than 0.5 mm when verified with subsequent histology. Latencies of evoked potential amplitude peaks are reported as mean ± SE milliseconds poststimulus, and comparisons of latencies were made using paired t-test with significance set to P 
0.05.
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A cytochrome oxidase (CO)-stained section through layer IV of the flattened right hemisphere of one animal was obtained to reveal the location and spatial extent of granular (dark) and dysgranular (light) regions to be provide a template for subsequent illustration of array placements in relation to these regions. The animal was perfused intracardially with 0.1 M phosphate buffer followed by modified peridata-lysine-paraformalehyde fixative (pH 7.4). Before the removal of the brain, a sucrose buffer solution was rinsed through the animal. To obtain a complete section of layer IV, the naturally curved cortex was flattened (Welker and Woolsey 1974) and immersed in a 30% sucrose buffer solution and kept at 7°C for 48 h. Sections were cut tangential to the pia with a cryotome at a thickness of 40 µm. Sections were incubated at 37°C in the dark for 1 h. The incubation medium was prepared immediately before use with 50 mg dimethyl sulfoxide and 5 g sucrose dissolved in 100 ml 0.1 M phosphate buffer. Before the introduction of the tissue sections, 95% O2-5% CO2 was also bubbled in the solution for 1 min. Incubation was terminated when differentiation between highly reactive and nonreactive areas could be discerned. Sections were rinsed in three changes of 0.1 M phosphate buffer, mounted, air dried, and coverslipped.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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) and auditory (Barth and Di 1991; Barth et al. 1993; Di and Barth 1992) cortex and was used to identify these regions throughout the remaining study. Normalized and interpolated (bi-cubic spline) maps of the initial positive amplitude peak of the SEP beginning at the earliest latency (Fig. 1D; 19 ms) and progressing in 1-ms steps to the longest latency (Fig. 1D; 25 ms) indicated the separate loci of primary cortex in the PMBSF (Fig. 1D; C2) and secondary cortex (Fig. 1D; c2) activated by stimulation of the contralateral C2 vibrissa. Because of its precisely localized response and reproducibility across animals, short-latency SEPs to C2 stimulation were used to functionally align the surface array in all subsequent recordings. At the medial array location depicted in Fig. 1, maps of the short latency primary SEP response that were averaged across animals (Fig. 2B; C2; 18.4 ± 1.4 ms) corresponded closely with the loci of peak SEP amplitudes for the individual animals (Fig. 2B; circles), centered on the C2 barrel of the PMBSF. Peak SEP amplitudes for the secondary C2 response (Fig. 2C; c2; 24.8 ± 2.6 ms) showed a similarly tight grouping. Subsequent maps of the primary short-latency SEP response to stimulation of the contralateral pinna (Fig. 2D; PN; 22.3 ± 0.7 ms), midtrunk (Fig. 2E; MT; 25.2 ± 0.6 ms), hindlimb (Fig. 2F; HL; 27.8 ± 1.2 ms), hindpaw (Fig. 2G; HP; 28.4 ± 1.3 ms), forelimb (Fig. 2H; FL; 23.5 ± 0.8 ms), and forepaw (Fig. 2I; FP; 23.1 ± 1.2 ms) indicated loci at more medial locations outside of the PMBSF and within the somatic representation of SI. A composite view of these responses (Fig. 2A) indicated an inverted somatotopic organization of primary cortex, with C2 (50% amplitude solid isocontour line and lettering color coded in black), PN (red), MT (orange), and HL (dark green) aligned along the lateral to medial axis, and the FL (dark blue), FP (light blue), and HP (light green) positioned rostrally. In this and subsequent illustrations, uppercase letters with solid contour lines were used to denote primary sensory zones, and lowercase letters with dashed contour lines labeled secondary cortex. Color codes for the various stimulated body parts remain consistent unless otherwise indicated.
At a more lateral position of the recording array, SEPs averaged across animals revealed loci of SII (Fig. 3). Stimulation of the C2 vibrissa produced a delayed response approximately 2 mm lateral to the border of the PMBSF, suggesting a distinct and complementary area of SII (Fig. 3C) that was rostral and lateral to the region identified in Fig. 2. Similarly, secondary responses to fl (Fig. 3D), hl (Fig. 3F), and mt (Fig. 3H) revealed two separate islands located at rostrolateral and caudomedial regions of the array. At this location, secondary responses to both fp (Fig. 3E) and hp (Fig. 3G) could only be detected at the rostrolateral locus, and those associated with pn (Fig. 3I) were only detected in the caudomedial locus. For the purpose of anatomical reference, the earliest latency response of the AEPs is also shown (Fig. 3B) and was centered on primary auditory cortex. At the rostrolateral locus, poststimulus latencies of the secondary responses were significantly delayed compared with corresponding response latencies in primary cortex (delay in ms: c2 = 5.9 ± 2.1, P < 0.01; fl = 3.8 ± 1.1, P < 0.01; fp = 4.1 ± 1.9, P < 0.05; hl = 4.6 ± 1.5, P < 0.01; hp = 5.2 ± 2.5, P < 0.05; mt = 8.0 ± 3.5, P < 0.01). Poststimulus latencies of secondary responses at the caudomedial locus were also significantly delayed compared with corresponding primary responses (delay in ms: fl = 3.6 ± 1.0, P < 0.01; hl = 4.8 ± 1.6, P < 0.01; mt = 7.5 ± 3.2, P < 0.01; pn = 5.0 ± 1.6, P < 0.01), but in no cases were there significant differences between the rostrolateral and caudomedial response latencies where they co-occurred (i.e., fl, hl, and mt). A composite diagram (Fig. 3A) indicated a great deal of overlap within the two regions of SII, obscuring their somatotopic organization. This was exacerbated by poor coverage of the array over the caudomedial region. However, the rostrolateral region revealed a rough somatotopic arrangement, with fl and fp positioned rostral to hl, hp, and mt.
A more posterior positioning of the electrode array provided better coverage of posterior SII (Fig. 4). Here, both the rostrolateral and caudomedial areas of secondary C2 cortex may be seen to be concurrently activated (Fig. 4C). Posterior secondary regions of fl (Fig. 4D), fp (Fig. 4E), hl (Fig. 4F), hp (Fig. 4G), mt (Fig. 4H), and pn (Fig. 4I) were more clearly delineated. Again, secondary responses were significantly delayed compared with corresponding primary responses but did not significantly differ in latency between the caudomedial and rostrolateral locus when both were activated. In addition, both the primary auditory response (Fig. 4B; AUD) and secondary response (Fig. 4B; aud) could be discerned and were in close agreement with previously published reports (Barth and Di 1990, 1991; Brett et al. 1994; Di and Barth 1992, 1993). Despite the remaining spatial overlap in the posterior SII responses, an approximate somatotopic organization was suggested in the composite (Fig. 4A), with rostral body parts positioned rostral to the caudal body parts.
During the multisensory interaction paradigm, auditory stimuli were presented at the beginning of the 100-ms recording epoch and somatosensory stimuli at a 50-ms delay. Auditory and somatosensory stimuli were presented either separately or in tandem to test for the effect of auditory stimuli on the subsequently evoked ASEP (auditory/somatosensory evoked potential). Figure 5A depicts a grand average across animals of the SEP response in SII to forepaw stimulation alone (Fig. 5A; black traces) with maximum amplitude in the rostral and extreme lateral region of the array. When auditory stimuli were presented alone, the grand average AEP (Fig. 5A; red traces) covered the primary auditory cortex but also spread rostrally (Fig. 5A; dashed red contour line = 25% peak amplitude of AEP), partially overlapping the separately evoked SEP response (Fig. 5A; dashed black contour line = 25% peak amplitude of SEP). A model (Fig. 5D; blue), computed as the sum of the separately evoked SEP and AEP, closely resembled the SEP alone (Fig. 5B) since the AEP complex at this latency was attenuated (Fig. 5C). However, when somatosensory stimuli were preceded by auditory stimuli in the same trials, multisensory interaction was evident. A preceding auditory stimulus both attenuated the subsequently evoked ASEP and increased its poststimulus latency (Fig. 5D; green trace) compared with the sum of the separately evoked responses. This deviation in ASEP response pattern from a sum of the AEP and SEP indicates neuronal interaction between the auditory and somatosensory stimulus, since, without interaction, the volume currents would simply sum linearly. Multisensory interaction was quantified at each electrode site by subtracting the summed unimodal responses (MODEL) from the response to combined stimulation (AUD/SOM), yielding a difference waveform (Fig. 5E; DIFF). In the example in Fig. 5, a normalized map of the maximum amplitude of this difference waveform (Fig. 5F) indicated that multisensory interaction included the forepaw representation of SII, but was more widespread, including caudal regions where the unimodal AEP and SEP spatially overlapped.
Maps of multisensory interaction, computed in this way for stimulation of other body regions (Figs. 6 and 7), displayed a similar pattern. Interaction was apparent in responses recorded from both the rostrolateral and caudomedial regions of SII and for every body region stimulated. Loci of multisensory interaction generally followed the pattern established for separately evoked SII responses. However, these regions were more widespread than corresponding secondary SEP responses. In addition, loci of multisensory interaction were shifted toward auditory cortex compared with the corresponding loci of maximum unisensory responses in SII. This is particularly apparent in composite maps of Fig. 8, where direct comparisons can be made between the somatotopic regions of SII (Fig. 8A) and multisensory interaction zones (Fig. 8B). While the somatotopic organization of multisensory foci in the caudal area of SII was still discernible, that in the rostral area was distorted, primarily by a shift of the forepaw and forelimb representations from their rostral location to more caudal and medial loci that were closer to auditory cortex.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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The topography of SI, derived here from SEP maps, agrees well with previous anatomical and electrophysiological studies in the rat (Chapin and Lin 1984; Hall and Lindholm 1974; Koralek et al. 1990; Wallace 1987; Welker 1971, 1976; Woolsey and LeMessurier 1948), mouse (Angel and Lemon 1975; Wallace 1987; Woolsey 1967), and squirrel (Krubitzer et al. 1986), indicating an inverted ratunculus.
Early latency and large amplitude components of the primary SEP response are accompanied by longer latency and smaller amplitude responses clustered in two distinct islands positioned 2-3 mm lateral to the primary response, suggesting two separate areas of SII. The most rostral of these areas (SIIrost) corresponds to classically defined SII in the rat (Akers and Killackey 1978; Chapin and Lin 1984; Fabri and Burton 1991; Koralek et al. 1990; Wallace 1987; Welker and Sinha 1972; Woolsey and LeMessurier 1948) and mouse (Carvell and Simons 1986, 1987; Wallace 1987; Woolsey 1967). Spatial overlap of evoked responses in this region makes detailed determination of its somatotopic organization difficult. However, at least on the rostrocaudal axis, a topographic organization is evident, with the forelimb and forepaw positioned rostral to the hindlimb and hindpaw representations. Positioning of the hindlimb, midtrunk, and forelimb lateral to the hindpaw representation (forepaw overlapped too much with forelimb to make a clear distinction) suggests an image of the rat's body that is upside down, similar to previous somatotopographic maps using evoked potential (Woolsey 1952; Woolsey and LeMessurier 1948) and microelectrode unit recordings (Welker and Sinha 1972). Location of the secondary representation of the C2 vibrissa is consistent with more complete evoked potential mapping of the major vibrissae (Barth et al. 1993; Di et al. 1994), indicating a large vibrissa representation of SII just lateral to the PMBSF (Carvell and Simons 1986, 1987; Fabri and Burton 1991; Koralek et al. 1990). Curiously, we were unable to record secondary responses to pinna stimulation in SIIrost, despite the substantial responses detected in SIIcaud. This may reflect an incomplete somatotopic representation in SIIrost or inadequate sampling of the area due the presence of the temporal bone. We are presently performing labeling studies of intracortical pathways between electrophysiologically identified areas of primary somatosensory cortex and SIIrost and SIIcaud that may help to clarify this issue.
There are several striking differences between the present responses from SIIrost recorded here and previous studies of SII. In a recent examination of ipsilateral cortical connections of SI, Fabri and Burton (1991) described somatotopically organized reciprocal connections between SI and two mirror image areas of secondary cortex, one just lateral to the PMBSF that they termed SII and a second inverted image located more laterally near the rhinal fissure termed the parietoventral (PV) area. We detected no distinct PV representation using evoked potential mapping. While this may attributed in part to the relatively poor spatial resolution of field potentials due to volume conduction, the trunk and proximal limb representations in their mirror image maps are separated by 
1 mm, which should be resolvable with the present mapping technique. As noted earlier, we may have missed part of PV due to its extreme lateral location, beyond the borders of our craniectomy, which stopped at the temporal bone. However, it is interesting to note that their trunk representation in PV is similar to our midtrunk representation in SIIrost. Their trunk representation in SII is placed near the caudal border of the PMBSF, similar to other studies (Carvell and Simons 1986, 1987; Koralek et al. 1990; Woolsey 1967), and close to the midtrunk representation of SIIcaud in this study. Thus a possible explanation for discrepancies between the present and past descriptions of SII topography is that previous reports may have combined into one composite secondary somatosensory zone, parts of what we have defined as a clearly separate somatotopic map in the SIIcaud.
In all SEP maps of this study, both SIIrost and SIIcaud are evident, each with its own topography. Secondary-evoked responses in SIIcaud are often of equal or larger amplitude than in SIIrost, particularly for the pinna and midtrunk, but separate responses for each body region under examination reveal separate secondary loci in rostral and caudal zones. The location and somatotopic organization of SIIcaud in the rat is quite similar to "SII" defined for the squirrel by Krubitzer et al. (1986), with their separately identified PV corresponding in location and approximate somatotopic organization to the present SIIrost in the rat. Given the consistently large responses to somatosensory stimulation that are evident in SIIcaud, it is puzzling why this region is rarely noted in previous studies of the rat. This may reflect in part a methodological advantage of high resolution evoked potential mapping, where widespread cortical regions can be simultaneously mapped and spatiotemporal differences in the SEP may be exploited to uniquely identify and separate activated regions.
However, this area has not gone unnoticed. Small injections of fluorescent tracers, particularly into the trunk or distal limb zones of SI, label a distinct parietal lateral region (PL; Fabri and Burton 1991) that corresponds closely with our SIIcaud. The same injections concurrently label regions within the SIIrost, suggesting dual representations in these areas. In a similar study, injections of tracer into the SI hindpaw area, which also appear to have spread into portions of the forepaw and trunk areas, labeled cells in SIIrost, but less dense label was also found farther caudomedially where we have identified SIIcaud (Koralek et al. 1990). While these authors attributed the caudomedial label to diffusion of the tracer injection onto the SI trunk representation, in light of the present results, these data may have actually reflected separate representation of the limbs as well as the trunk in SIIcaud. In the present results, the forelimb, pinna, midtrunk, and hindpaw representation within SIIcaud is positioned at progressively more caudal locations, indicating a somatotopic organization oriented similar to that of SIIrost. Whether the secondary response to C2 vibrissa stimulation, positioned caudal to the PMBSF, represents a complementary vibrissa representation of SIIcaud cannot be stated with any certainty without more systematic vibrissa mapping, which was not performed here. An alternative explanation is that it may lie within anterior extrastriate cortex where neurons that respond to whisker deflection as well as visual stimuli have been detected in mice (Wagor et al. 1980) and may therefore belong to a separate body map.
SEPs from both SIIrost and SIIcaud spatially overlap click-evoked AEPs, which is evident in the rostral and medial belt areas of auditory cortex (Patterson 1977), suggesting that cells in these regions may have multisensory response properties (Barth et al. 1993, 1995; Brett-Green et al. 2003; Di et al. 1994). This possibility is confirmed by spatiotemporal interactions observed between the AEP and SEP when auditory and somatosensory stimuli are presented in tandem. Combined stimulation always produces a response that differs from the linear sum of separate auditory and somatosensory responses, with the greatest interaction evident near auditory cortex where the AEP and SEP maximally overlap (for a notable exception to this general rule, the multisensory c2 response is actually shifted slightly away from the c2 response to unimodal stimulation in SIIrost). Maps of these interaction patterns indicate that both SIIrost and SIIcaud have the capacity to participate in multisensory integration, a conclusion that is consistent with a recent report from our laboratory describing a multisensory zone (MZ) in rat cortex that extends along the border between primary auditory cortex and the PMBSF (Brett-Green et al. 2003). This general organizational pattern of multisensory cortex occupying the transitional areas between primary sensory cortices has also been noted in other recent microelectrode studies of the rat (Wallace et al. 2004).
While our previous work concentrated only on interactions between auditory- and vibrissa-evoked responses, the present results extend these findings to spinal representations of SII. The involvement of SIIrost in multisensory integration is consistent with earlier electrophysiological studies in the rodent (Carvell and Simons 1986, 1987; Koralek et al. 1990; Welker and Sinha 1972; Welker et al. 1988; Woolsey 1967), indicating that spinal representation within classically defined (rostral) SII is responsive to auditory stimulation. The present finding that SIIcaud also responds to auditory stimulation might have been anticipated from previous examination of thalamocortical input to this region (Brett-Green et al. 2003). Injection of small quantities of retrograde tracer into a region overlapping what we now know as the pinna, midtrunk, forelimb, and forepaw region of SIIcaud, labels cells in the ventral posterior lateral (Vpl) and posterior (Po) nuclei of somatosensory thalamus as well as the ventral and medial divisions of the medial geniculate (MGv and MGm, respectively) and the suprageniculate (Sg) nuclei of acoustic thalamus. Thus while SIIcaud may receive sparse intracortical projections from SI (Fabri and Burton 1991; Koralek et al. 1990), it has access to both somatosensory and auditory afferent input via direct thalamocortical pathways. A similar picture may apply to SIIrost, which has well-defined intracortical projections from SI (Fabri and Burton 1991; Koralek et al. 1990). The loci of multisensory interactions in SIIrost, at the rostral border of primary auditory cortex, overlaps the secondary auditory belt cortex. SIIrost therefore probably receives direct auditory input from the acoustic thalamus (Arnault and Roger 1990; Brett et al. 1994; Patterson 1977; Ryugo and Killackey 1974; Winer and Larue 1987) as well as input from the somatosensory thalamus (Tracey and Waite 1995).
The function of SII in general, and consequently the differential function of SIIrost versus SIIcaud identified in this study, is largely unknown. Due to the wider and largely overlapping receptive fields in SII compared with SI, it may be plausible that SII serves as a higher stage in the processing of somatosensory information (Killackey 1983), serving to integrate information across broader body regions and possibly to integrate submodalities of somatosensation segregated in SI. However, evidence from this study indicates that another function of SII, and that of secondary cortex in other sensory modalities, is in the parallel processing of features concerned with multisensory integration. Ipsilateral connections between SI and SII are not unidirectional from primary to secondary, but reciprocal. It is apparent, at least in the rat, that SII receives as much if not more thalamic input as it does from SI (Brett-Green et al. 2003), suggesting a role in parallel processing as well as in hierarchical processing. While multisensory regions are shifted slightly toward the border of auditory cortex, they are partially co-localized with SIIrost and SIIcaud, respectively, suggesting that many but not all cells in these zones perform multisensory integration. It can only be speculated why there are two separate regions of SII in the rat and what their functional differences might be. It is interesting to note that SIIcaud identified here is adjacent to and partially overlaps a region of secondary visual cortex in the rat that responds to both visual and auditory stimuli (Barth et al. 1995), which was recently confirmed by Wallace et al. (2004). Thus in general, substantial subregions of the secondary sensory cortices might be sites of augmented responsiveness to a combination of sensory stimuli. In the specific case of SIIrost versus SIIcaud, the difference could be in the integration of bimodal (som/aud) versus trimodal (som/aud/vis) stimuli, respectively. The fact that, in the rat, there are two separate SII regions could be viewed as an expression of the overwhelming importance of somatosenses for this species.
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ACKNOWLEDGMENTS |
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This research was supported by National Institute of Neurological Disorders and Stroke Grant R01 NS-36981.
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FOOTNOTES |
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Address for reprint requests and other correspondence: D. S. Barth, Dept. of Psychology, Univ. of Colorado, Campus Box 345, Boulder, CO 80309-0345 (E-mail: dbarth{at}psych.colorado.edu).
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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Angel A and Lemon RN. Sensorimotor cortical representation in the rat and the role of the cortex in the production of sensory and myclonic jerks. J Physiol 248: 465-488, 1975.
Arnault P and Roger M. Ventral temporal cortex in the rat: connections of secondary auditory areas Te2 and Te3. J Comp Neurol 302: 110-123, 1990.[CrossRef][ISI][Medline]
Barth DS and Di S. Three dimensional analysis of auditory evoked potentials in rat neocortex. J Neurophysiol 64: 1527-1536, 1990.
Barth DS and Di S. The functional anatomy of auditory evoked potentials in rat neocortex. Brain Res 565: 109-115, 1991.[CrossRef][ISI][Medline]
Barth DS, Goldberg N, Brett B, and Di S. The spatiotemporal organization of auditory, visual, and polysensory evoked potentials in rat cortex. Brain Res 678: 177-180, 1995.[CrossRef][ISI][Medline]
Barth DS, Kithas J, and Di S. Anatomic organization of evoked potentials in rat parietotemporal cortex: somatosensory and auditory responses. J Neurophysiol 69: 1837-1849, 1993.
Brett B, Di S, Watkins L, and Barth DS. An HRP study of parallel thalamocortical projections responsible for the generation of mid-latency auditory evoked potentials. Brain Res 647: 65-75, 1994.[CrossRef][ISI][Medline]
Brett-Green B, Fifkova E, Larue DT, Winer JA, and Barth DS. A multisensory zone in rat parietoremporal cortex: intra- and extracellular physiology and thalamocortical connections. J Comp Neurol 460: 223-237, 2003.[CrossRef][ISI][Medline]
Carvell GE and Simons DJ. Somatotopic organization of the second somatosensory area (SII) in the cerebral cortex of the mouse. Somatosens Mot Res 3: 213-237, 1986.
Carvell GE and Simons DJ. Thalamic and corticocortical connections of the second somatic sensory area of the mouse. J Comp Neurol 265: 409-427, 1987.[CrossRef][ISI][Medline]
Chapin JK and Lin CS. Mapping the body representation in the SI cortex of anesthetized and awake rats. J Comp Neurol 229: 199-213, 1984.[CrossRef][ISI][Medline]
Di S and Barth DS. Topographic analysis of field potentials in rat vibrissa/barrel cortex. Brain Res 546: 106-112, 1991.[CrossRef][ISI][Medline]
Di S and Barth DS. The functional anatomy of middle latency auditory evoked potentials: thalamocortical connections. J Neurophysiol 68: 425-431, 1992.
Di S and Barth DS. Binaural vs. monaural auditory evoked potentials in rat neocortex. Brain Res 630: 303-314, 1993.[CrossRef][ISI][Medline]
Di S, Brett B, and Barth DS. Polysensory evoked potentials in rat parietotemporal cortex: auditory and somatosensory responses. Brain Res 64: 267-280, 1994.
Fabri M and Burton H. Ipsilateral cortical connections of primary somatic sensory cortex in rats. J Comp Neurol 311: 405-424, 1991.[CrossRef][ISI][Medline]
Hall RD and Lindholm EP. Organization of motor and somato-sensory neocortex in the albino rat. Brain Res 66: 23-28, 1974.
Killackey HP. The somatosensory cortex of the rodent. Trends Neurosci 6: 425-429, 1983.[CrossRef]
Koralek KA, Olavarria J, and Killackey HP. Areal and laminar organization of corticocortical projections in the rat somatosensory cortex. J Comp Neurol 299: 133-150, 1990.[CrossRef][ISI][Medline]
Krubitzer LA, Sesma MA, and Kaas JH. Microelectrode maps, myloarchitecture, and cortical connections of three somatotopically organized representations of the body surface in the parietal cortex of squirrels. J Comp Neurol 250: 403-430, 1986.[CrossRef][ISI][Medline]
Patterson H. An Anterograde Degeneration and Retrograde Axonal Transport Study of the Cortical Projections of the Rat Medial Geniculate Body. Boston, MA: Boston University, 1977.
Ramachandran R, Wallace MT, Clemo HR, and Stien BE. Multisensory convergence and integration in rat cortex. Soc Neurosci Abstr 19: 1447, 1993.
Ryugo DK and Killackey HP. Differential telencephalic projections of the medial and ventral divisions of the medial geniculate body of the rat. Brain Res 82: 173-177, 1974.[CrossRef][ISI][Medline]
Tracey DJ and Waite PME. Somatosensory system. In: The Rat Nervous System (2nd ed.), edited by Paxinos G. San Diego, CA: Academic Press, 1995, p. 689-704.
Wagor E, Mangini NJ, and Pearlman AL. Retinotopic organization of striate and extrastriate visual cortex in the mouse. J Comp Neurol 193: 187-202, 1980.[CrossRef][ISI][Medline]
Wallace MN. Histochemical demonstration of sensory maps in the rat and mouse cerebral cortex. Brain Res 418: 178-182, 1987.[CrossRef][ISI][Medline]
Wallace MT, Ramachandran R, and Stein B. A new view of sensory cortical parcellation. Proc Natl Acad Sci USA In press.
Welker C. Microelectrode delineation of fine grain somatotopic organization of SmI cerebral neocortex in albino rat. Brain Res 26: 259-275, 1971.[CrossRef][ISI][Medline]
Welker C. Receptive fields of barrels in the somatosensory neocortex of the rat. J Comp Neurol 166: 173-190, 1976.[CrossRef][ISI][Medline]
Welker C and Sinha MM. Somatotopic organization of SmII cerebral neocortex in albino rat. Brain Res 37: 132-136, 1972.[CrossRef][ISI][Medline]
Welker C and Woolsey TA. Structure of layer IV in the somatosensory neocortex of the rat: description and comparison with the mouse. J Comp Neurol 158: 437-454, 1974.[CrossRef][ISI][Medline]
Welker E, Hoogland PV, and Van der Loos H. Organization of feedback and feedforward projections of the barrel cortex: a PHA-L study in the mouse. Exp Brain Res 73: 411-435, 1988.[ISI][Medline]
Winer JA and Larue DT. Patterns of reciprocity in auditory thalamocortical and corticothalamic connection: study with horseradish peroxidase and autoradiographic methods in the rat medial geniculate body. J Comp Neurol 257: 282-315, 1987.[CrossRef][ISI][Medline]
Woolsey CN. Patterns of localization in sensory and motor areas of the cerebral cortex. In: Milbank Symposium, The Biology of Mental Health and Disease. New York: Hoeber, 1952, p. 193-206.
Woolsey CN and LeMessurier DH. The pattern of cutaneous representation in the rat's cerebral cortex. Fed Proc 7: 137, 1948.
Woolsey TA. Somatosensory, auditory and visual cortical areas of the mouse. Johns Hopkins Med J 121: 91-112, 1967.[ISI][Medline]
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