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Symposium Reports |
1 Departments Neurobiology and Biomedical Engineering, Center for Neuroengineering, Duke University Durham, NC 27710, USA
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Abstract |
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(Received 24 January 2005;
accepted after revision 29 April 2005;
first published online 5 May 2005)
Corresponding author M. A. L. Nicolelis: Box 3209, Room 327 Bryan Research Building, Duke University, Durham, NC 27710, USA. Email: nicoleli{at}neuro.duke.edu
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Introduction |
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TopAbstractIntroductionReferences |
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By employing multielectrode recordings in freely behaving rats we have recently obtained physiological and behavioural data supporting the hypothesis that the thalamocortical loop dynamically adjusts its physiological mode of operation, at both cellular and circuit levels, in accordance with internal brain states and the specific behaviours used by rats to explore their surrounding environment. Here, we briefly review the evidence that supports this hypothesis. A series of papers published elsewhere summarizes this argument in greater detail (Nicolelis & Fanselow, 2002; Krupa et al. 2004a; Gervasoni et al. 2004).
The rat somatosensory thalamocortical circuit
Figure 1 summarizes the circuit that defines the main thalamocortical loop of the trigeminal component of the rat somatosensory system (Fig. 1A). Ascending action potentials resulting from mechanical stimulation of the whiskers travel to the trigeminal brainstem complex and the reticular formation. Projections from the trigeminal brainstem complex terminate on neurones in the VPM thalamus. In the rat, the VPM thalamic nucleus contains only one type of neurone, excitatory cells that project mainly to layer IV (CTX IV) of the primary somatosensory cortex (SI). On the way to the cortex, the axons of VPM also give off a projection to the thalamic reticular nucleus (RT). VPM and RT neurones also receive dense ascending cholinergic projections from the brainstem reticular formation (RF) (Hallanger et al. 1987). These projections can excite VPM cells through nicotinic and M1-type muscarinic receptors (Zhu & Uhlrich, 1998; Plummer et al. 1999), but inhibit RT cells via M2-type receptors (Carden & Bickford, 1999).
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Although considerable anatomical and physiological data indicate that top-down inputs may have a significant effect on mechanisms of tactile information processing (Mignard & Malpeli, 1991; Roelfsema et al. 1998; Hupe et al. 1998), the nature of these descending influences even on the primary thalamocortical loop of the rat somatosensory system remains poorly understood. As a rat actively samples a tactile stimulus, particularly one involving salient associative memories, several higher-order processes that would not be activated by random passive stimuli, delivered in either anaesthetized or paralysed animals, will likely be engaged. For instance, the animal's state of attention, motivation, sensory-motor integration and reward expectation are all likely to influence the nature of the tactile responses generated by thalamocortical neurones. However, what effect these, or other, higher-order processes might have on mechanisms of tactile processing in rat SI remains largely unknown.
Over the past decade, our laboratory has performed a series of experiments in which chronic recordings of the simultaneous activity of ensembles of thalamocortical neurones were obtained in freely behaving rats engaged in a variety of tasks (for a review see Nicolelis & Fanselow, 2002). In our first studies, we measured how the tactile responses of ensembles of single neurones located in S1 and VPM of the thalamus varied according to three basic behaviours exhibited by rats. The first of these we refer to as the ‘quiet’ behaviour, in which rats are standing or sitting still and there is no movement of the whiskers (Fanselow & Nicolelis, 1999; Nicolelis et al. 1995). The second is known as the ‘whisker twitching’ behaviour. During this behaviour, rats are also standing or sitting still, but twitch their whiskers in very rhythmic, small amplitude movements at a rate of 7–12 Hz (Semba et al. 1980; Semba & Komisaruk, 1984). The third behaviour, referred to as ‘whisking’, occurs when rats move their whiskers back and forth in large-amplitude sweeps at a rate of 
4–6 Hz. Rats use these whisking movements to repeatedly put their whiskers in contact with surfaces or objects so they can gather tactile information as they actively explore their environment (Carvell & Simons, 1990). During the quiet and whisking behaviours, there is no large-scale, coherent neural activity among the cells in either VPM or SI, and the activity is thus referred to as ‘desynchronized’. In contrast, the whisker twitching state is accompanied by a highly synchronous 7–12 Hz oscillatory neural activity (Semba et al. 1980; Semba & Komisaruk, 1984) (Fig. 2A), which appears first in the rat SI cortex and later in the VPM thalamus (Nicolelis et al. 1995; Fanselow et al. 2001). Shortly after the onset of this oscillatory neural activity in the thalamocortical loop, rats start producing the rhythmic, small amplitude whisker twitching movements characteristic of this behaviour, which are phase-locked to the neural oscillations (Semba & Komisaruk, 1984; Welker, 1964).
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75 ms during the quiet behaviour. This poststimulus inhibitory period is shorter during whisker twitching, relative to the quiet behaviour, and is substantially shorter during whisking (Fig. 2C). Finally, when pairs of stimuli are presented, the ability of a neurone to fire in response to the second stimulus in the pair is dependent on the interstimulus interval and the animal's behavioural state. During the quiet and whisker twitching behaviours, if the interstimulus interval is less than 75 ms, the probability of VPM and SI neurones responding to the second stimulus in a pair will be very small (Fig. 2B). However, during whisking, the probability of a response to the second stimulus of a pair is only reduced if the interstimulus interval is 25 ms or less. Thus, the ability of VPM and SI neurones to respond reliably to rapidly repeated stimuli is correlated with the duration of the poststimulus inhibitory period, which differs according to behavioural state. Analysis of the firing properties of thalamocortical cells (Fanselow et al. 2001) in these behaving rats has shown that during the 7–12 Hz oscillations observed in the whisker twitching behaviour, VPM and S1 neurones fire bursts of action potentials substantially more frequently (average of once every 7.2 s) than during the quiet (average of once every 45.5 s) or whisking (average of once every 28.6 s) behaviours (Fig. 2D). Moreover, signals directed from SI to VPM are significantly more coherent during whisker twitching episodes than during the other two behavioural states (Fig. 2E). In addition, inactivation of the SI cortex via local infusion of the GABAA agonist muscimol, abolished whisker twitching movements, 7–12 Hz oscillations and bursting activity in the VPM. These results suggest that during whisker twitching the SI cortex exerts a powerful rhythmic influence on VPM neurones and that these descending cortical signals are required for the emergence of 7–12 Hz oscillations, the bursting activity observed in VPM during these oscillations, and the genesis of the whisker twitching behaviour.
These results led us to propose that the active use of whiskers, in multiple types of whisker movements, is integral to processing tactile stimuli in rats. Indeed, our hypothesis proposes that two distinct types of whisker movements serve as differential dynamic ‘filters’ to process specific types of incoming tactile information that result from whisker stimulation. The second global operating principle we proposed is that, as with the determination of receptive field properties and maps in SI and VPM (Krupa et al. 1999; Ghazanfar et al. 2001), the asynchronous convergence of ascending and descending projections in the thalamus is critical for generating the animal's range of sensory processing strategies. When this circuit arrangement is combined with the range of intrinsic cellular properties of cells in the thalamocortical loop, a complex and dynamic system emerges, which is capable of quickly shifting its physiological properties in order to maximize the type of tactile information sampled by a particular active exploratory behaviour. Finally, we hypothesized that internal changes in brain state would significantly impact on the way ensembles of thalamocortical neurones respond to incoming tactile stimuli.
Together, these principles illustrate that the rat somatosensory system does not merely play the role of a ‘passive observer’ of the environment. Instead, it can choose from multiple functional modes in order to actively examine and analyse tactile inputs from the world, based on expectations built throughout a life of whisking.
Layer specific tactile responses in the rat S1 during active tactile discrimination
A recent series of experiments further highlighted the profound differences in tactile information processing that exist across the layers of the S1 cortex when rats engage themselves in active whisker discrimination, versus serving as passive recipients of comparable tactile stimuli (Krupa et al. 2004a). In these experiments, Krupa et al. recorded the activity of ensembles of single neurones through different layers of the barrel region of S1 in five rats that were trained to perform a whisker-dependent tactile discrimination task (Krupa et al. 2001b, 2004b). The task required rats to actively sample a variable-width aperture with their large facial whiskers, and then signal whether the aperture was ‘narrow’ or ‘wide’ (Fig. 3A). Video analysis showed that rats approached and sampled the aperture in a very repeatable, stereotypical manner, using only their large facial whiskers to contact the aperture (Fig. 3B). Single-unit activity was recorded through all layers of SI with chronically implanted, movable arrays of high impedance microwire electrodes. Electrodes were orientated perpendicular to the cortical surface so that recordings along an individual electrode track were from the same cortical column. This allowed neural activity recorded at different depths through individual cortical columns to be compared.
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These responses were compared with the activity of 244 units recorded in the S1 of 10 additional rats that received several different forms of passive whisker stimulation designed to simulate the spatio-temporal dynamics of whisker deflections that occurred during the active discrimination. Three of the rats received patterned ramp-and-hold stimulation of 16 individual whiskers with a multichannel whisker stimulator (Krupa et al. 2001a, 2004b) while lightly anaesthetized (Fig. 4A). Three rats were habituated to calm, head-fixed restraint and received similar, patterned ramp-and-hold stimuli (Fig. 4A) while fully awake (Wiest & Nicolelis, 2003; Krupa et al. 2004b). Four rats received bilateral whisker stimulation with a movable aperture while lightly anaesthetized or restrained and fully awake (Fig. 4B). This moving aperture (same size as the aperture in the active discrimination) was accelerated across the facial whiskers at velocities and trajectories that replicated the whisker deflection dynamics that occurred during active discrimination (Krupa et al. 2004b).
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In contrast, passive ramp-and-hold whisker stimulation (in either anaesthetized or awake, restrained rats) or moving aperture stimulation (in anaesthetized or awake rats) evoked excitatory responses that consisted of relatively brief, transient increases in activity (Fig. 4D and E). The mean excitatory response durations and magnitudes evoked by these passive stimuli are summarized in Fig. 4F. Response duration during active discrimination was highly significantly different from each of the passive stimulation conditions (F4,85 = 59.2, all P < 0.0005; Tukey's HSD. The same was true of the response magnitude measure (F4,85 = 29.9, all P < 0.00001, Tukey's HSD. In short, excitatory activation of S1 by passive whisker stimulation was fundamentally different in nature than S1 excitation evoked by the active discrimination. Several additional lines of evidence indicate that this shift from phasic to tonic activation during passive and active stimulation (as well as several other functional differences, described below) could not have resulted solely from variations in whisker deflection dynamics during passive and active stimulation (Krupa et al. 2004b).
Another functional difference between active and passive stimulation was a significant shift in the relative balance between excitatory and inhibitory responses. Only 7% of S1 units responded to the ramp-and-hold or moving aperture passive stimulation with either purely inhibitory responses or inhibitory followed by excitatory activation; the remaining 92% responded with either purely excitatory or excitatory followed by inhibitory activity, results consistent with earlier studies (Simons, 1978; Swadlow, 1989; Brumberg et al. 1999; Sachdev et al. 2000). Moreover, there was no significant difference in the percentage of inhibitory responses evoked by the different passive stimuli delivered to either anaesthetized or awake, restrained rats. In contrast, nearly half (49%) of S1 units responded during the active discrimination with either a purely inhibitory response (26%) or a response that was initially inhibitory followed by an excitatory phase (23%). The mean duration of inhibitory responses during the active discrimination (246 ± 21 ms) was significantly longer than the duration of inhibitory responses evoked by the passive stimuli (12.4 ± 1.8 ms); (t(12) = 9.9, P < 0.0001). During active discrimination, purely inhibitory responses were evenly distributed across layers: 33% in supragranular layers, 36% in layer IV and 31% in infragranular; inhibitory–excitatory responses were asymmetrically concentrated in the granular layer: 23% in supragranular, 54% in layer IV, and 23% in infragranular. Collectively, these different inhibitory responses indicate that the activation dynamics of S1 following passive whisker stimulation are fundamentally different from during active discrimination. Passive multiwhisker stimulation causes a predominately excitatory deviation from prestimulus baseline activity, whereas similar stimulation during active discrimination evokes almost equally balanced excitatory and inhibitory shifts from baseline.
The functional nature of these actively evoked inhibitory responses was examined using an artificial neural network, based on the learning vector quantization (LVQ) algorithm (Krupa et al. 2004b). Results revealed that information about different aperture widths is encoded simultaneously by excitatory and inhibitory responses in S1 (see LVQ Based Analyses in Krupa et al. 2004b). Further, LVQ-analysis of ensemble activity in different layers indicates that layer-specific tactile coding mechanisms may be engaged during active discrimination. For instance, single-trial prediction of wide and narrow apertures by infragranular ensembles was significantly more accurate than supragranular ensembles (Krupa et al. 2004b).
Finally, cortical columns displayed significantly different functional properties during active discrimination and passive stimulation. S1 recordings in monkeys, cats, and rats show that responses within a column evoked by passive stimulation share similar functional properties of place (all units have a common receptive field locus), and mode (all units respond to similar stimulus modalities) (Mountcastle, 1957; Powell & Mountcastle, 1959; Simons, 1978; Chapin, 1986; Armstrong-James et al. 1992; Brumberg et al. 1999). In contrast, during the active discrimination described here, 36% of infragranular units began responding significantly before the rats' whiskers contacted the aperture during active discrimination. More importantly, these units began responding significantly earlier than units recorded directly above them in supragranular or granular layers (Fig. 5A). Onset latencies between supragranular and granular layers did not differ significantly (Fig. 5B). In contrast, onset latencies of infragranular units were significantly earlier than units in the more superficial layers (Tukey's HSD, P < 0.0005).
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In summary, numerous functionally significant differences in S1 activity were observed in different cortical layers as rats performed an active tactile discrimination (Fig. 5C). Moreover, fundamental differences in the functional nature of S1 activity were observed during active discrimination and passive whisker stimulation. These results suggest that S1 receives significantly different afferent input during actively acquired and passively delivered stimuli. These differences do not appear to result exclusively from changes in bottom-up ascending input to S1. Instead, during active discrimination, top-down influences may also affect tactile processing in S1. For instance, the early onset units were only observed in infragranular layers and not layer IV, indicating that these responses did not arise from ascending thalamic input. Because motor cortex (M1) sends a significant projection to S1 infragranular layers (Miyashita et al. 1994; Zhang & Deschenes, 1998), these early onset responses might represent modulation from MI as rats initiate the discrimination. Also, excitatory response durations and magnitudes in supra- and infragranular layers were substantially greater than those in layer IV during active discrimination, indicating that the non-granular laminae received additional excitatory input from sources other than ascending thalamocortical input. Possible sources of this input include the secondary somatosensory cortex (Koralek et al. 1990; Jackson & Cauller, 1998) and the contralateral SI (Olavarria et al. 1984; Koralek et al. 1990; Shuler et al. 2001; Shuler et al. 2002), both of which innervate the non-granular laminae.
Conclusions
Evidence obtained under a variety of experimental conditions indicates that tactile responses produced by ensembles of S1 and VPM vary according to the animal's behavioural strategy and internal brain state. Functional differences observed in the rat thalamocortical loop during active versus passive stimulation also indicate that passively evoked tactile responses constitute a relatively poor predictor of the processing mechanisms operating in the mammalian somatosensory system during active discrimination.
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Footnotes |
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