We observed speeded RTs and somatosensory-evoked responses when a TMS pulse was delivered to the somatomotor network 15–40 ms after a median nerve stimulus. Largest facilitatory effects were observed when the TMS pulse was targeted at the contralateral SII at about 20 ms post-stimulus.
Previous studies utilizing human intracranial recordings have shown SII activity beginning already at 15–27 ms post-stimulus, which is simultaneous or earlier than onset of the SI activity (Barba et al., 2002
). Therefore, SII must receive direct early parallel sensory input independent of the pathway via SI, consistent with the current and earlier (Karhu and Tesche, 1999
) MEG observations.
Speeded RTs for TMS at early post-stimulus latencies have been described before (Gregori et al., 2005
), thus supporting our behavioral results. However, these effects have been attributed to multisensory redundancy caused by the auditory click from the stimulator coil, largely because in these studies the RT effect has been similar regardless of the TMS target area (Gregori et al., 2005
; Walsh and Pascual-Leone, 2003
). Our results show TMS site specificity and therefore are not compatible with this interpretation. To examine this further, we made control measurements in one subject where the auditory click from the TMS coil was identical but the TMS-evoked currents were reduced by over 50% (sham coil). The TMS pulse was given 21 ms after the somatosensory stimulus. The subject did not know when real vs. sham TMS was used. RTs were significantly faster for real vs. sham stimulation over cSII (p<
0.05) and iMI (p<
0.001) but not over cSI (p<
0.15); iSII was not tested. Both TMS site specificity and the control measurement therefore support the idea that the speeded RTs were caused by TMS-evoked neuronal currents.
We propose that the speeded RTs can be best explained if the somatosensory-evoked physiological SII activation at about 20 ms normally exerts a top–down SII→SI influence that facilitates the reciprocal SI→SII pathway. With TMS to SII at ~20 ms, it appears that we amplified a brain-speeding mechanism already in place. This interpretation is supported with the current findings of site specificity of TMS and ERP latency shifts already at the SII level.
More generally, fast thalamocortical parallel sensory inputs to multiple cortical sites could drop the activation thresholds of the cortico-cortical connections between the areas (Ullman, 1996
). This mechanism could almost immediately after a stimulus establish a widespread network where the nodes receiving parallel input would be likely to communicate with each other.
Theoretical and physiological studies have suggested that top–down effects may facilitate and guide the reciprocal bottom–up flow, even though the cellular-level mechanisms are still poorly known (Siegel et al., 2000
; Ullman, 1995
). However, in order to be effective, top–down processes should be running already when the bottom–up stream is finding its way towards higher levels of cortical hierarchy (Ullman, 1996
). This is obviously difficult to achieve with serial processing. One possibility is that the brain utilizes serial pathways specialized for very fast information transfer to initiate early activity in high-order association cortices. For example, visual recognition has been shown to utilize early top–down influences from orbitofrontal cortex initiated by fast serial (via V1) magnocellular pathways (Bar, 2003
; Bar et al., 2006
; Kveraga et al., 2007
). The somatosensory data are inconsistent with serial processing models because activations start earlier in SII than SI. The current study therefore offers an appealing alternative mechanism: association cortices could receive direct thalamocortical sensory input, allowing simultaneous top–down and bottom–up processing. Both mechanisms may well coexist.
The idea of parallel thalamocortical sensory inputs to multiple cortical areas may appear inconsistent with the view that transmission of sensory information is hard wired from the thalamic sensory nucleus to the corresponding sensory projection cortex. However, first-order thalamic nuclei receiving driving input from sensory organs are reciprocally connected with and heavily modulated by both higher-order thalamic nuclei (e.g., pulvinar) and cortex, reflecting attentional and other task-related demands (Guillery and Sherman, 2002
; O′Connor et al., 2002
; Sherman, 2007
; Sherman and Guillery, 1996
; see Bender and Youakim, 2001
; Briggs and Usrey, 2007
; Zikopoulos and Barbas, 2007
for recent related work in primates). Pulvinar, on the other hand, has massive reciprocal connections throughout the neocortex (e.g., Adams et al., 2000
; Buchsbaum et al., 2006
; see Shipp, 2003
for a review). The cortex can thus receive fast sensory input from the thalamus directly from the first-order thalamic nucleus (when such pathways exist) or through a higher-order thalamic area such as the pulvinar. Modulating inputs to thalamic nuclei could in a dynamic manner adjust which cortical areas receive parallel sensory input.
Given that both association and low-level sensory cortices appear to receive very early parallel crossmodal inputs (Fort et al., 2002
; Foxe and Schroeder, 2005
; Giard and Peronnet, 1999
; Molholm et al., 2002
; Murray et al., 2005
; Schroeder and Foxe, 2002
; Schroeder et al., 2003
), some via the pulvinar (Budinger et al., 2006
; Hackett et al., 2007
), a similar mechanism as suggested in the current study could also explain why reaction times to multisensory stimuli are faster than to unisensory stimuli (Raab, 1962
; Schröger and Widmann, 1998
). Early physiological SII activations may also serve a protective function due to the roles of SII in pain processing (Timmermann et al., 2001
) and sensorimotor integration (Forss and Jousmäki, 1998
; Huttunen et al., 1996
It has been suggested that serial processing is more prevalent in higher primates, and there seems to be an evolutionary shift in mammals where humans have the least amount of parallel sensory inputs to higher-order areas (Coleman et al., 1999
; Kaas and Garraghty, 1991
; Zhang et al., 2001
) and therefore increased serial processing of sensory input. Thus, it appears that in the course of evolution humans may have traded some processing speed for better cognitive control.
From the large number of trials and consistent results across subjects, it follows that the current results are reliable within the studied population, but due to limited access (the instruments were located on different continents), our number of subjects was small. Hence, more studies with larger subject populations are needed to estimate how abundant this mechanism is.