Organization of Somatosensory Areas I and II in Marsupial Cerebral Cortex: Parallel Processing in the Possum Sensory Cortex

G. T. Coleman, H. Q. Zhang, G. M. Murray, M. K. Zachariah, and M. J. Rowe

School of Physiology and Pharmacology, The University of New South Wales, Sydney 2052, Australia


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Coleman, G. T., H. Q. Zhang, G. M. Murray, M. K. Zachariah, and M. J. Rowe. Organization of somatosensory areas I and II in marsupial cerebral cortex: parallel processing in the possum sensory cortex. Controversy exists over the organization of mammalian thalamocortical somatosensory networks. An issue of particular contention is whether the primary and secondary somatosensory areas of cortex (SI and SII) are organized in a parallel or serial scheme for processing tactile information. The current experiments were conducted in the anesthetized brush-tail possum (Trichosurus vulpecula) to determine which organizational scheme operates in marsupials, which have taken a quite different evolutionary path from the placental species studied in this respect. The effect of rapid reversible inactivation of SI, achieved by localized cortical cooling, was examined on both evoked potential and single neuron responses in SII. SI inactivation was without effect on the amplitude, latency, and time course of SII-evoked potentials, indicating that the transient inputs responsible for the SII-evoked potential reach SII directly from the thalamus rather than traversing an indirect serial route via SI. Tactile responsiveness was examined quantitatively before, during, and after SI inactivation in 16 SII neurons. Fourteen were unchanged in their responsiveness, and two showed some reduction, an effect probably attributable to the loss of a facilitatory influence exerted by SI on a small proportion of SII neurons. The temporal precision and pattern of SII responses to dynamic forms of mechanical stimuli were unaffected, and temporal dispersion in the SII response bursts was unchanged in association with SI inactivation. In conclusion, the results establish that, within this marsupial species, tactile inputs can reach SII directly from the thalamus and are not dependent on a serially organized path through SI. A predominantly parallel organizational scheme for SI and SII operates in this representative of the marsupial order, as it does in a range of placental mammals including the cat and rabbit, the tree shrew and prosimian galago, and at least one primate representative, the marmoset monkey.


    INTRODUCTION
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

In most mammals, each sensory system, whether somatosensory, visual, or auditory, is characterized by multiple representations within the cerebral cortex. For the tactile system, two of the principal cortical processing regions are somatosensory area I (SI) and area II (SII), (for reviews see Burton 1986; Felleman and Van Essen 1991; Johnson 1990; Jones 1986; Kaas 1987; Rowe 1990a). It is probable that corresponding areas are present in marsupials as SI and SII were identified in the possum (Adey and Kerr 1954; Haight and Neylon 1978) and the opossum (Beck et al. 1996; Lende 1963a,b, 1969; Pubols 1977; Pubols et al. 1976) although the forelimb area is substantially smaller in SII than in SI.

As both SI and SII receive direct anatomic projections from the ventroposterior (VP) nucleus of the thalamus in both primate and nonprimate placental mammals (for review see Jones 1985) and in marsupials (Haight and Neylon 1978; Pubols 1968), it was usually assumed that the cortical mechanisms in tactile sensation depend on parallel, distributed processing (Mountcastle 1978; Rowe 1990a). Direct evidence in support of the parallel processing hypothesis was obtained in a diverse range of placental mammals, including cat (Burton and Robinson 1987; Mackie et al. 1996; Manzoni et al. 1979; Turman et al. 1992), rabbit (Murray et al. 1992), tree shrew, and the prosimian galago (Garraghty et al. 1991), as SI inactivation in these species has little effect on SII tactile responsiveness. In contrast, it was found that in simian primates SII responsiveness is abolished by surgical ablation of SI (Burton et al. 1990; Garraghty et al. 1990; Pons et al. 1987, 1992). This dependency of SII responsiveness on SI provided evidence for a serial scheme in which tactile information is conveyed from the thalamus to SI and then to SII via intracortical connections (Garraghty et al. 1990; Pons et al. 1987, 1992). These findings in support of a serial processing scheme led to the hypothesis that there are fundamental differences between simian primates and other eutherian mammals in the organization of thalamocortical systems for tactile processing (Garraghty et al. 1991; Mackie et al. 1996; Murray et al. 1992; Turman et al. 1992). However, our recent re-investigation of SI-SII organization in the marmoset, with localized cooling for SI inactivation, demonstrated a substantial direct thalamic input to SII, indicating a parallel organization of SI and SII in this primate species (Rowe et al. 1996; Zhang et al. 1996). This study extends the analysis of parallel versus serial processing in SI and SII to the brush-tail possum, Trichosurus vulpecula, a representative of the marsupial order that has taken a divergent evolutionary path from placental mammals ~100 million years ago in the Cretaceous period (Rowe 1990a). The aim was to determine whether there was evidence for parallel organization of SI and SII at this early stage of mammalian evolution (see DISCUSSION). The study was reported in abstract form (Coleman et al. 1997).


    METHODS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Eighteen experiments were performed on the brush-tail possum, T. vulpecula. In four, examining principally the effect of SI inactivation on SII-evoked potentials, anesthesia was induced with either ketamine (20-60 mg/kg) and xylazine (2-6 mg/kg) or Saffan (alfaxalone and alfadolone acetate; Glaxo; 18 mg/kg), and maintained with chloralose (20 mg/kg iv initial dose and as needed). In the remainder, 4 were with ketamine and xylazine anesthesia (doses as described previously) and maintained with pentobarbitone (~2-4 mg kg-1 h-1 iv), and 10 were with initial Saffan anesthesia (18 mg/kg im) and maintenance with pentobarbitone (1 mg kg-1 h-1 iv) and ventilation mixture of halothane (~1-2%), N2O (~80%), and oxygen (20%). Experiments were terminated by pentobarbitone overdose and were approved by the university animal ethics committee (Approval No. ACE 94/77) and accorded with the Australian Code of Practice for the Care and Use of Animals for Scientific Purposes.

Rectal temperature for this marsupial was maintained at ~36°C. The femoral artery and vein were cannulated, and a tracheal cannula was inserted. A unilateral craniotomy was performed to expose the somatosensory cortical areas. A paraffin pool (36°C) was created to prevent the cortex from drying. The distal forelimb contralateral to the craniotomy was fixed in a perspex trough to allow reliable placement of the mechanical stimulator on the receptive fields of cortical neurons.

Mapping of distal limb representations in SI and SII

The distal forelimb areas within SI and SII were mapped by surface recording of evoked potentials with a ball electrode. Areas of representation were identified from short-latency (<15 ms) positive-going evoked potentials generated by brief taps (3- to 5-ms duration; 400-µm amplitude) to the central palmar surface of the contralateral forelimb.

Inactivation of the SI hand area by cooling

A cylindrical silver block (5- to 7-mm diam) fitted with a Peltier device and a thermistor was placed over the SI hand area of cortex. The temperature at the block face was held at 36-37°C but could be lowered within 1-2 min to <10°C and restored equally rapidly to the control temperature. The effectiveness of this procedure for rapid reversible inactivation of localized regions of somatosensory cortex was established by Brooks (1983) and in our earlier studies (Mackie et al. 1996; Murray et al. 1992; Turman et al. 1992, 1995; Zhang et al. 1996).

Evoked potentials were recorded simultaneously from SI, with an electrode in the face of the cooling block and with a second electrode from the forelimb representation within SII. Evoked potentials were averaged (20-40 successive responses) by a laboratory computer. Inactivation of the SI area was judged to have taken place when the SI evoked potential was abolished (usually at <= 10°C). The effect of SI inactivation on SII responsiveness was evaluated by recording evoked potential and single neuron responses within SII.

Recording and stimulation procedures for single neuron studies

Conventional extracellular recording was carried out from individual tactile-sensitive neurons within the SII hand area (Zhang et al. 1996). Receptive fields of tactile-sensitive SII neurons were delineated by gentle tapping with a small probe or with von Frey hairs. Quantified mechanical stimuli generated by a servo-controlled mechanical stimulator (Zhang et al. 1996) were delivered with circular probes (2- to 4-mm diam) at a rate of one per 8-10 s to allow recovery of skin position.

Individual SII neurons were tested for responsiveness to static skin displacement or trains of either sinusoidal vibration or rectangular pulses. The effect of SI inactivation on SII neurons was evaluated wherever possible by comparison of responsiveness during inactivation with both pre- and postinactivation controls. For each neuron, the comparison was based on statistical analysis involving one-way ANOVA, and the source of differences was identified by contrast analysis (Duncan test; P < 0.05 for significance) (Snedecor and Cochran 1989).


    RESULTS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Identification of distal forelimb regions of SI and SII in the possum

Two spatially separate representations of the contralateral hand, within the SI and SII areas identified by Adey and Kerr (1954), were found by evoked potential mapping. The SI hand area, typically 5-7 mm in anteroposterior extent and 4-5 mm in mediolateral extent, was in the medial region of cortex (Fig. 1).



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Fig. 1. Identification by evoked potential mapping of somatosensory areas I and II of possum cortex. Hand representations within SI and SII were determined by recording short-latency, positive-going evoked potentials from the cortical surface in response to a brief (3 ms) tap stimulus, delivered to the contralateral palm. A: right side of the possum brain, modified from Fig. 1B in Haight and Neylon (1978). The SI and SII hand areas (medial and lateral shaded areas respectively in A) were defined as the areas where short-latency, positive-going evoked potentials (B) were recorded from the cortical surface (in recording rows 1-4 for SI, and 8-10 for SII in A and B). Potentials recorded along rows 1-6 (2-mm spacing) and rows 7-11 (1-mm spacing) in B were recorded at the cortical sites marked in A. Each trace is the average of 20 successive responses to the tap stimulus (duration 3 ms, amplitude 200 µm) delivered 10 ms after the onset of each sweep. The SII hand area mapped in this particular experiment was slightly larger than usual.

The SII representation of the contralateral hand was in the lateral margin of the parietal cortex (Fig. 1) just above sulcus beta  (Haight and Neylon 1978). Its size was consistently smaller than its SI counterpart and rarely larger than 2-3 mm across its broadest dimension. The representation of the contralateral face (Adey and Kerr 1954) created a discontinuity between the SI and SII hand representations, with an average separation of ~8 mm between the nearest boundaries of the SI and SII hand areas, enabling cooling-induced inactivation of SI to be achieved without direct spread of cooling causing significant disruption to neural activity within the SII hand area (see Turman et al. 1992).

Inactivation of the SI hand area by localized cooling

As the temperature of the SI block face was reduced in a series of 5-6°C steps from 36°C, there was a progressive reduction in amplitude of the SI-evoked potential and an increase in latency to its positive peak (Fig. 2). The attenuation of the SI response was apparent once the temperature fell to ~25°C, with marked reduction and slowing by 16°C. In all 10 experiments in which the effectiveness of cooling was evaluated in this stepwise manner, the SI-evoked potential was abolished by cooling to 5-10°C. In some experiments, there was a small residual positive-going SI response apparent at short latency at these low temperatures (e.g., at 5 and 11°C in Fig. 2), almost certainly attributable to activity in the thalamocortical input fibers (see Turman et al. 1992; Zhang et al. 1996). With stepwise rewarming to 36°C there was progressive recovery of the SI response (Fig. 2), confirming the reversibility of the procedure in the possum as in placental mammals (Turman et al. 1992; Zhang et al. 1996).



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Fig. 2. Reversible inactivation of SI by means of localized cooling and its effect on SII evoked potentials. Effect of cooling of the SI hand area on evoked potentials recorded simultaneously from the focus of the hand areas of SI (left) and SII (right). The inactivation sequence involved cooling the surface of SI progressively in ~5-6°C steps from 36 to 5°C, followed by a stepwise rewarming. The SI-evoked potential was abolished at 5°C, but there was no effect on the SII-evoked potential or its time course. Each trace is the average of 20 successive responses to the tap stimulus; duration 3 ms, amplitude 200 µm; onset at arrow. For this and other observations on the effects of SI cooling on evoked potential or single neuron responses, the SI temperature was held at each setting for >= 1 min before starting the assessment.

Effect of SI inactivation on evoked potentials recorded from SII

Inactivation of the SI hand area was without effect on the amplitude, latency, and time course of SII-evoked potentials in the 13 experiments where this was examined. This is illustrated for two experiments (Figs. 2 and 3A) where, despite the marked delay and attenuation of the SI response as the SI temperature fell and the abolition of the SI response at 5-10°C, there was no change in the SII response. This was confirmed in Fig. 3, B and C, by the quantified plots of peak amplitude and onset latency for the SII-evoked response in association with the decline and disappearance of the SI-evoked potential. Furthermore, the time course of the SII evoked potential appears unchanged (Figs. 2 and 3) despite the marked delay in the time course of the attenuated SI response at the lower SI temperatures. Further evidence that the SII-evoked potential is generated by direct thalamic input rather than by signals traversing an indirect serial route via SI comes from the absence of any significant difference in onset latencies of the simultaneously recorded SI- and SII-evoked potentials (13.6 ± 1.7 ms (SD) and 13.0 ± 1.8 ms (SD), respectively; P = 0.41; n = 15). In these 15 experiments onset latencies were the same in 1 case and marginally shorter for SI in 5 cases and for SII in 9 cases.



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Fig. 3. Effect of SI inactivation on onset latency and peak amplitude of SI and SII evoked potentials. A: evoked potentials recorded over the SI and SII hand areas as the temperature of SI was progressively dropped from 37 to 8°C. Each trace is the average of 20 successive responses to the tap stimulus (duration 3 ms, amplitude 200 µm) delivered 10 ms after the onset of each 100-ms sweep. Vertical scale bar is 50 µV for both SI and SII traces. B and C plot the onset latencies (ms) and peak amplitudes (µV), respectively, of the SI- and SII-evoked potentials as a function of SI temperature. Values plotted for the SI- and SII-evoked potentials were the averaged responses obtained during the cooling (shown in A) and rewarming sequences. The onset latency of the SI evoked potential increased progressively as the SI temperature was lowered, and the SI peak amplitude decreased until the evoked potential was abolished at 8°C. However, the onset latency and peak amplitude of the SII-evoked potential were unaffected.

Effect of SI inactivation on responsiveness of individual SII neurons

As the evoked potential is generated by an abrupt transient input, it may take place before contributions can be made to the SII response over a putative indirect serial path via SI. It was therefore necessary to examine the effects of SI inactivation on the responses of single SII neurons to maintained tactile stimuli that would allow any contributions coming over an indirect path to be manifest.

Quantitative single-neuron analysis was completed for 16 SII neurons with tactile receptive fields on the distal forelimb. In none was there an abolition of responsiveness in association with SI inactivation. In all but 2 of 16 SII neurons tested statistically for an effect of SI inactivation on responsiveness there was no evidence of any consistent effect. The failure of SI inactivation to alter responsiveness of SII neurons to tactile stimuli is shown for two neurons in Fig. 4. The graphs in Fig. 4, A and B, plot the response level to a fixed stimulus as a function of time during the stepwise cooling of SI leading to complete inactivation at 5-6°C. They also show the subsequent recovery of SI transmission as the SI temperature was restored in a similar stepwise sequence.



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Fig. 4. Absence of effect of SI inactivation on the responsiveness of 2 SII neurons. A and B plot the response level (impulses/s) for 2 SII neurons responding to successive repetitions of a fixed tactile stimulus applied to the region of peak sensitivity in their receptive fields on the glabrous skin proximal to digit 5. Both cells were activated most effectively by low-frequency rectangular pulses (in each case, at 2.7 Hz, 275 µm amplitude) superimposed for 1 s on a 1.5-s step indentation (amplitude 200 µm). Response levels are plotted as a function of time, and the temperature of the cortical surface at SI was progressively cooled in ~5° steps from 37 to 5°C as indicated by the temperature records forming A and B, top traces.

In Fig. 4A, the mean response (± SD) of the SII neuron to a train of mechanical pulses was 5.7 ± 1.0 imp/s (n = 23) during the period of SI inactivation (SI at 5°C), a response level that was unchanged (i.e., P > 0.05) from the pre- and postcooling control levels of 5.7 ± 0.9 imp/s (n = 10) and 5.8 ± 1.1 imp/s (n = 20), respectively, obtained when the SI surface temperature was 37°C. In Fig. 4B, the response level, plotted for another SII neuron, was again unchanged by SI inactivation. The mean response when SI was inactivated (at 5-6°C) was 6.9 ± 2.1 imp/s (n = 16), which was not significantly different from the pre- and postcooling levels of 6.9 ± 4.6 imp/s (n = 11) and 6.3 ± 1.3 imp/s (n = 10) respectively.

All 16 SII neurons tested failed to display a maintained response to static indentations of the skin and were purely dynamically sensitive. They were activated by abrupt mechanical perturbations in the form of low-frequency rectangular pulse trains. The traces in Fig. 5A show an SII neuron responding with a spike burst to the ON and OFF phases of the rectangular mechanical pulses in both pre- and postcooling control circumstances (SI at 37°C) and where SI was inactivated (7°C). The graph in Fig. 5B plots the response level to successive repetitions of the stimulus while two SI inactivation sequences took place. Although the neuron displayed considerable moment-to-moment variability in responsiveness and some drift in response level over time, there was no consistent change in association with SI inactivation. This was apparent from the statistical tests where the mean (± SD) precooling control response (11.2 ± 4.4 imp/s; n = 20) was not significantly different from the level during the first period of SI inactivation (12.3 ± 8.4 imp/s; n = 14). Although the postcooling control response was statistically higher than that during the first inactivation period, it was also statistically higher than the precooling control, reflecting the upward drift in response level over the first ~10 min of sampling. During the later sampling period there was a downward drift in responsiveness that gave a statistical difference between response levels in the second inactivation period and its immediately preceding control segment but not between this second inactivation period and its postcooling control (see Fig. 5 legend). The data emphasize the importance of reversible inactivation that permits repetition of the inactivation to test for the consistency of effects. In cases such as Fig. 5 there is insufficient consistency to accept a systematic effect of SI inactivation on SII responsiveness.



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Fig. 5. Absence of effect of SI inactivation on an SII neuron. A: impulse records are shown of the response of an SII neuron to stimulation of its receptive field on the pad of the forepaw, proximal to digit 4, with low frequency (2.7 Hz, 225 µm amplitude) rectangular pulses, superimposed for 1 s on a 1.5-s background step indentation (amplitude 200 µm). The neuron responded to each of the ON and OFF, phases of the rectangular pulses with bursts of 2-3 action potentials during both pre- and postcooling controls and when SI was inactivated by cooling to 7°C. B: response levels (impulses/s) of the same neuron to successive repetitions of the fixed tactile stimulus are plotted as a function of time, whereas SI was inactivated twice by cooling the cortical surface to 7°C. The average response (± SD) during the 3 control segments was 11.2 ± 4.4, 17.3 ± 3.8, and 13.4 ± 2.5 impulses/s, respectively, and during the 2 segments of SI inactivation was 12.3 ± 2.9 and 12.3 ± 3.2 impulses/s, respectively. There was no statistically significant difference in the response of neuron during the precooling control and the first cooling run (P > 0.05). Although there was a significant difference between the first cooling run and its postcooling control, there was also a significant difference between the precooling control and the first postcooling control, reflecting a drift in excitability and responsiveness over this period unrelated to the SI inactivation. There was no significant difference between the response level in the second cooling run and the level during the second postcooling control (P > 0.05). Responses obtained during the transition phases of cooling or rewarming were not included in the comparisons.

In only 2 of 16 SII neurons was there any evidence for an effect of SI inactivation on responsiveness. Data for the more convincing of these two cases is illustrated in Fig. 6 where three repetitions of the inactivation procedure produced a fall in response level. Although there was considerable moment-to-moment fluctuation in response level, the statistical tests, comparing the response level during each inactivation segment with the immediately preceding and succeeding control levels, revealed a significant change (P < 0.05) in four of the six comparisons (see Fig. 6 legend).



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Fig. 6. Reduced responsiveness in an SII neuron in association with SI inactivation. Responses of an SII neuron (imps/s) are plotted as a function of time in response to successive repetitions of a 1.5-Hz train of rectangular pulses (amplitude 1 mm), delivered for 1 s to the receptive field of the neuron on the dorsal (hairy skin) region of digit 1. The SI hand area was inactivated by cooling to ~9°C during 3 successive cooling runs. The 4 separate control response levels (± SD) were 3.6 ± 1.1, 4.3 ± 1.7, 4.0 ± 1.7, and 4.6 ± 1.5 impulses/s, respectively, whereas levels during each of the 3 inactivation periods were 2.6 ± 1.0, 2.4 ± 1.3, and 3.0 ± 2.1 impulses/s, respectively. Comparison of the response of the neuron during each cooling run with its immediate pre- and postcooling controls revealed a difference between "inactivation" and control values (P < 0.05) for 4 of 6 comparisons. Perhaps related to the considerable moment-to-moment variability in the neuron's response, there was no significant difference (P > 0.05) between the first control and first cooling segments or between the penultimate control and third cooling segments.

Effect of SI inactivation on temporal patterning in the SII responses to repetitive mechanical stimuli

We also examined the effect of SI inactivation on the pattern of SII responses to the repetitive mechanical stimuli. This pattern of activity could change with SI inactivation if inputs to SII were mediated via both direct and indirect (via SI) paths from the thalamus. The peristimulus time histograms in Fig. 7, constructed before (A), during (B), and after (C) SI inactivation from the responses of an SII neuron to mechanical pulse stimuli, show no evidence in association with SI inactivation of a change in response level or in the temporal distribution of impulse activity to the onset and offset phases of the rectangular pulses.



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Fig. 7. Effect of SI inactivation on the distribution of impulse activity in SII responses to repetitive mechanical pulse stimuli. Peristimulus time histograms were constructed from 10 successive responses of an SII neuron to repetitions of a 2.7-Hz train of rectangular pulses (225 µm amplitude, superimposed on a 1.5-s step of 200 µm) applied to the glabrous skin of the forepaw proximal to digits 4 and 5, before (A), during (B), and after (C) inactivation of SI by cooling the cortical surface to 8°C. The grouping of impulse activity appears unchanged during SI inactivation in B compared with pre- and postcooling controls in A and C.

More precise evaluation of the timing of the response to the mechanical stimuli was achieved by constructing cycle histograms (Fig. 8), which show the probability of spike occurrence at different points throughout the cycle period of the mechanical pulse train. Impulse traces in Fig. 8, A-C, show a burst of spikes at the onset and offset phases of each mechanical pulse. However, the cycle histograms show that the timing relations of these spike bursts are unchanged in Fig. 8B when SI was inactivated (5°C) compared with the control distributions in A and C and that the dispersion in the bursts is also unchanged by SI inactivation. The expanded spike waveforms verify that the identical SII unit was studied before (SI at 37°C), during (SI at 5°C), and after (SI at 37°C) SI inactivation. The absence of any prolongation in the SII spike waveform when SI was at 5°C also confirms that there was no spread of cooling to the SII recording site (see Zhang et al. 1996).



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Fig. 8. Absence of effect of SI inactivation on temporal patterning in SII responses to repetitive mechanical pulse stimuli. Impulse traces in A-C, left side, show the responses of an SII neuron to the onset and offset phases of the repetitive mechanical pulse stimulus (2.7 Hz; 275 µm amplitude, delivered on a background 1.5 s, 200 µm step indentation to the glabrous skin proximal to digit 5) before (A), during (B), and after (C) SI inactivation induced by cooling to 5°C. The cycle histograms on the right side were constructed in each case from 10 consecutive responses and show the precise timing relations and dispersion in the spike activity in relation to the cycle period (~370 ms) of the 2.7-Hz mechanical stimulus. The expanded superimposed spike waveforms (5 in each of the 1-ms duration traces) for the SII neuron show that there was no slowing of the spike when SI was inactivated and confirms therefore that there was no significant direct spread of cooling to SII.


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Effect of SI inactivation on SII-evoked potential responses

As SII evoked potentials were unaffected by SI inactivation, one may conclude that this feature of SII responsiveness, based as it is on a synchronous afferent volley generated by a brief tap stimulus, cannot be dependent on inputs that traverse an indirect serial path from the thalamus via SI. If thalamocortical organization in the possum conformed to a strict serial scheme, the prolongation of the SI-evoked potential and its increase in latency, in the course of SI cooling, must lead to a comparable delay and prolongation of the SII-evoked potential. As this was not observed, the inputs responsible for this transient SII response presumably transverse a direct path from the thalamus to SII. The almost identical onset latencies for the SI- and SII-evoked potentials also suggest that the inputs project directly to each area over parallel pathways. Furthermore, as there was no effect of SI inactivation on the late components of the SII-evoked potential (e.g., Fig. 2), there was no evidence for the SII response being generated by both a direct (thalamic) and an indirect (via SI) source of input. In these respects the evoked potential results for the possum are similar to those obtained in the cat, rabbit, and marmoset monkey (Murray et al. 1992; Turman et al. 1992; Zhang et al. 1996).

Effect of SI inactivation on responsiveness of individual SII neurons

Quantitative single neuron analysis established that SII responses to skin stimulation are mediated via a direct projection from the thalamus independent of SI. Even for the neurons (2/16) that displayed some fall in response in association with SI inactivation, it is probable that the reduction was not attributable to loss of a component of the peripherally generated input that traversed an indirect route from the thalamus to SII via SI. Instead it may reflect the loss of a background facilitatory influence that arises in SI and is mediated via the intracortical path from SI to SII, in agreement with our earlier observations in placental mammals (Murray et al. 1992; Turman et al. 1992, 1995; Zhang et al. 1996). It should also be emphasized that the small fall in responsiveness in these two SII neurons cannot be attributed to direct spread of cooling from the SI cooling site as the separation of the SII recording site from the cooling block was substantial (>8 mm) (see Turman et al. 1992).

Thalamocortical connectivity and the organization of the SI and SII areas in the possum

Much controversy over how SI and SII are organized in placental mammals has persisted despite the recognition that, in all placental species examined, there are direct anatomic projections from the thalamus to both SI and SII, an anatomic arrangement that would suggest a parallel organization. In the case of the possum, Haight and Neylon (1978) established that the SI area coincides with the anatomic projection field of the VP thalamic nucleus. Although their tracer studies identified a projection of VP neurons to SII, the incidence of these SII-related neurons was rather sparse, a finding that could be taken as evidence that the principal path for tactile inputs to SII might be via an indirect route from VP via SI. However, the current findings provide little support for this interpretation and confirm that tactile information traverses a direct path from the thalamus to SII. The sparse distribution of SII-related VP neurons in the possum probably reflects the small size of the SII forelimb area vis-à-vis its SI counterpart in marsupials (Adey and Kerr 1954; Beck et al. 1996; Lende 1963a,b, 1969; Pubols 1977; Pubols et al. 1976). Nevertheless, the finding of SII-related cells in VP, although sparse, establishes an anatomic substrate for a direct thalamocortical input to SII that is consistent with the present findings.

Parallel organization of SI and SII in different species

Earlier studies from our laboratory and elsewhere demonstrated parallel organization of SI and SII in a diverse range of nonprimate placental mammals (Burton and Robinson 1987; Garraghty et al. 1991; Manzoni et al. 1979; Murray et al. 1992; Turman et al. 1992, 1995). In each of these species, SI inactivation had little effect on tactile responsiveness within SII. In contrast, in the macaque and marmoset monkeys SII responsiveness was abolished when SI was inactivated by surgical ablation, a result indicative of a serial scheme of processing (Garraghty et al. 1990; Pons et al. 1987, 1992), which led to the hypothesis that there are fundamental differences between simian primates and other placental mammals in the organization of thalamocortical systems for tactile processing (Garraghty et al. 1991; Murray et al. 1992; Turman et al. 1992). However, a recent reinvestigation of the serial-parallel processing issue for SI and SII in the marmoset monkey with localized cortical cooling for reversible inactivation of SI (Rowe et al. 1996; Zhang et al. 1996) demonstrated a very substantial, perhaps exclusive, parallel organization of SI and SII for tactile processing, indicating that the serial processing scheme is not necessarily an attribute of all primate species. Furthermore, the finding that SII responsiveness in the marsupial, T. vulpecula, survives SI inactivation demonstrates that the predominantly parallel organizational scheme also operates in mammals of the marsupial order that diverged from the placental line in the Cretaceous period, ~140-70 million years ago (Rowe 1990a). The current finding strengthens the case for parallel organization of SI and SII being a common ancestral feature at this early stage of mammalian evolution and therefore suggests that, in a phylogenetic sense, parallel processing is a very old strategy. An alternative interpretation would be that the parallel organization of SI and SII is sufficiently advantageous as a design strategy, that it has emerged independently as an example of parallel evolution in the separate placental and marsupial lines of mammalian evolution.

Although the parallel scheme appears to be the dominant organizational mode for SI and SII in most mammalian species in which systematic study was undertaken (Burton and Robinson 1987; Garraghty et al. 1991; Manzoni et al. 1979; Murray et al. 1992; Pons et al. 1987, 1992; Rowe et al. 1996; Turman et al. 1992, 1995; Zhang et al. 1996), including a variety of nonprimate placental mammals, the marmoset monkey, and now a marsupial representative, there is also the report of serial organization of SI and SII in the Old World simian primate, the macaque monkey (Pons et al. 1987,1992). The possible existence within the mammalian orders of both organizational modes therefore raises the issue of what advantages or disadvantages might be conferred on the animal by each of these organizational schemes. One advantage the parallel scheme could confer is an element of built-in redundancy, providing a more "fail-safe" mode of operation for the sensory system and making the system less susceptible to local disruptions. However, it must be emphasized that parallel organization of SI and SII need not mean redundancy in design of the processing network. First, quantitative aspects of processing may differ somewhat in SI and SII even where the same peripheral source of input is conveyed to both SI and SII (Ferrington and Rowe 1980; Fisher et al. 1983). Second, the output connections of SI and SII are not identical (Burton 1986; Friedman et al. 1986; Kaas 1993), and therefore even identical information processed in the two areas may be utilized for different perceptual or sensorimotor purposes. Thus parallel SI and SII processing sites may constitute dual-purpose systems, in contrast to a strict serial system in which both SI and SII constitute different stages of a single, hierarchically organized network. Furthermore, the simultaneity of their processing may serve to minimize "reaction times" for the animal. In contrast, a serial scheme may add temporal delays and extend "reaction time." A further disadvantage of a multistage serial processing scheme may be that some aspects of information processing, in particular, those that rely on temporal precision in impulse signaling, may be degraded as successive synaptic junctions are traversed in the processing path (e.g., see Ferrington and Rowe 1980; Rowe 1990b).

However, as possible compensation for these putative disadvantages, the serial processing scheme may allow more scope than the largely simultaneous parallel processing model for a time-dependent modulation or gating of sensory inputs at successive stages of the processing network.

Finally, it must be emphasized that, in view of our recent demonstration that a parallel organization of SI and SII does operate in the marmoset monkey, it may be important to re-investigate, with the same reversible-inactivation procedure, the issue of serial and parallel processing in SI and SII of the macaque monkey, in case the surgical ablation procedure for SI inactivation may have induced effects that confounded the interpretation of results in this primate species.


    ACKNOWLEDGMENTS

The authors acknowledge the technical assistance of C. Riordan and H. Bahramali, and the National Parks and Wildlife Service of New South Wales for permission to conduct studies on the possum.

This work was supported by the Australian Research Council and the National Health and Medical Research Council of Australia.


    FOOTNOTES

Address for reprint requests: M. J. Rowe, School of Physiology and Pharmacology, University of New South Wales, Sydney, N.S.W. 2052, Australia.

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Received 5 October 1998; accepted in final form 25 January 1999.


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