Vibrissal basal ganglia circuits

• Prof. Kevin Alloway, College of Medicine, Pennsylvania State University

In species such as rats and mice, the vibrissal basal ganglia circuit is a subcomponent of the sensorimotor channel in the basal ganglia network. As such, it consists of all regions in the basal ganglia that process vibrissa-related information received from the cortex. Like other components of the sensorimotor channel, the information processed by the vibrissal circuit comes mainly from the primary somatosensory (SI) and motor (MI) cortical areas. Like all functional channels in the basal ganglia, the vibrissal circuit contains input and output nuclei that are interconnected, both directly and indirectly. The processed output of the vibrissal circuit is sent to specific nuclei in the thalamus that project to the frontal cortical areas where motor decisions are made. Consistent with the role of the sensorimotor channel in selecting and executing behavioral movements, the available evidence suggests that the vibrissal circuit is involved in selecting and executing coordinated movements of the head, neck, and whiskers during a wide range of behaviors.

Many mammals have vibrissae, but only two marsupials (Virginia opossum, Brazilian short-tailed opossum) and a few rodents (e.g., mouse, rat, gerbil, hamster, chinchilla, manatee) actively move their whiskers in a directed manner to acquire tactile information about the spatial features of external objects (Rice, 1995). In all other species that have vibrissae (e.g., rabbit, cat, dog, squirrel, chipmunk, manatee), tactile information is acquired from passive whisker deflections that occur as the animal moves through space or as other objects move towards the animal’s head. Although the basal ganglia processes tactile information produced by passive stimulation of the whiskers, interest in using the whisker system as an animal model for understanding the functional organization of the basal ganglia has focused on the active whisking system of rats and mice.

Vibrissal basal ganglia connections

The vibrissal circuit has the same series of interconnections as in other functional channels of the basal ganglia. The neostriatum, which represents the input nucleus for the vibrissal circuit, receives vibrissal information from the cortical areas that evaluate sensory inputs from the peripheral whiskers. These corticostriatal projections originate from cortical layers III, V and VI, and they use glutamate as an excitatory neurotransmitter. Neostriatal medium spiny neurons, which are excited by the corticostriatal projections, use GABA as an inhibitory neurotransmitter and represent the source of all neostriatal efferent projections. One set of these neostriatal projections project directly to the basal ganglia output nuclei, the entopeduncular nucleus and the pars reticulata of the substantia nigra. The other set of neostriatal projections terminate in the lateral globus pallidus; this projection system represents the indirect pathway for conveying information to the output nuclei. In this indirect route, the GABAergic neurons in the lateral globus pallidus project to the subthalamic nucleus, which uses glutamate as an excitatory neurotransmitter in its projections to each of the output nuclei. Both output nuclei use GABA as an inhibitory neurotransmitter and project to motor-related regions in the thalamus, especially the ventromedial and ventrolateral nuclei, which project to the MI whisker region.

Vibrissal cortical areas

In rats and mice, whisker-related information is conveyed to SI cortex by two parallel pathways that originate in the brainstem and project to the contralateral thalamus. While projections from the principal sensory trigeminal (PrV) nucleus terminate in the ventroposteromedial (VPM) thalamus and form the lemniscal pathway, projections from the interpolaris division of the spinal trigeminal (SpVi) nucleus terminate in the medial part of the posterior (POm) thalamus and form the paralemniscal pathway. Both of these pathways convey information to the SI barrel field, which represents the main cortical target for processing vibrissal inputs (Woolsey and van der Loos, 1970; Welker, 1976). The lemniscal pathway terminates in the layer IV barrels, which contain high concentrations of cytochrome oxidase and, collectively, form an isomorphic map of the peripheral whisker pad. By comparison, the paralemniscal pathway terminates in the layer IV septa that separate individual barrels from each other.

As shown by Fig.<ref>F1</ref>, several cortical areas receive vibrissa-related inputs from the thalamus and SI barrel cortex. The secondary somatosensory (SII) cortex, for example, receives projections from VPM, POm, and SI barrel cortex (Carvell and Simons, 1987; Spreafico et al., 1987; Fabri and Burton, 1991). In addition, the parietal ventral cortex receives dense projections from SI barrel cortex (Fabri and Burton, 1991). The posterior parietal cortex receives projections from SI barrel cortex and POm, but not from VPM (Reep et al., 1994). All of these cortical areas, including SI barrel cortex, convey vibrissal information to the basal ganglia.

Figure 1: Feedforward connections between the cortical regions that convey vibrissal information to the basal ganglia. Cortical regions innervated by VPM or POm are color-coded red or green, respectively.

The MI whisker region also processes vibrissal-related information and conveys it to the neostriatum. Although the MI whisker region is operationally defined by the sites where microstimulation evokes twitches of the contralateral whiskers (Gioanni and Lamarche, 1985; Brecht et al., 2004), extracellular recordings demonstrate that mechanical whisker deflection reliably activates neurons in the deep layers of MI (Chakrabarti et al., 2008). As indicated by Fig.<ref>F1</ref>, the MI whisker region receives vibrissal information directly from POm and from multiple cortical areas including SI, SII, the parietal ventral region, and the posterior parietal cortex (Aldes, 1988; Alloway et al., 2004; Colechio and Alloway, 2009).

Vibrissal corticostriatal projections

The vibrissal circuit extends through all nuclei in the basal ganglia, but most studies of this functional channel have centered on the neostriatum, especially its dorsolateral region. Like other parts of the neostriatum, the dorsolateral region receives inputs from the substantia nigra pars compacta and the parafascicular nucleus in the intralaminar part of the thalamus (Alloway et al., 2006). In addition, the dorsolateral neostriatum also receives some thalamic inputs from the POm nucleus, which is part of the paralemniscal pathway for conveying whisker-related information to SI barrel cortex.

The dorsolateral neostriatum represents the part of the neostriatum that receives the densest inputs from SI barrel cortex (Brown et al., 1998; Alloway et al., 1999). The dorsolateral region also receives whisker-related corticostriatal projections from SII, the parietal ventral cortex, and the posterior parietal cortex (Levesque et al., 1996; Alloway et al., 2000; Alloway et al., 2006). The MI whisker region, which is located in medial agranular cortex (Brecht et al., 2004), has substantial connections with the neostriatum, many of which terminate in the dorsolateral region (Hoffer and Alloway, 2001). Detailed analysis of the projections from these different cortical regions has revealed several important principles of corticostriatal organization in the vibrissal and related sensorimotor circuits:

• Divergence: In all mammals, including primates, corticostriatal projections in the sensorimotor channel have a one-to-many projection pattern (Flaherty and Graybiel, 1991). This divergent pattern is also present in the vibrissal system, where projections from individual whisker-barrel columns in SI terminate in multiple, discontinuous patches in the dorsolateral neostriatum (Alloway et al., 1998). Divergent corticostriatal projections represent a mechanism for distributing the same sensorimotor information to multiple processing zones in the neostriatum.

• Convergence: Consistent with this one-to-many projection pattern, each neostriatal region receives overlapping inputs from several cortical sites. An early tracing study in primates, for example, indicates that interconnected cortical regions project to overlapping parts of the striatum (Yeterian and Van Hoesen, 1978). Although this pattern has exceptions (Selemon and Goldman-Rakic, 1985), corticostriatal projections from interconnected vibrissal regions are also characterized by large amounts of corticostriatal overlap (Alloway et al., 1999, 2000; Hoffer and Alloway, 2001).

• Somatotopic organization: The densest projections from the head, limb, and trunk representations in SI cortex terminate in distinct yet overlapping regions. Consequently, the neostriatum contains a rough somatotopic map in which the forepaw region is located ventral to the hindpaw region, and both limb representations tend to be medial and rostral to the main part of the vibrissal representation (Carelli and West, 1991; Brown, 1992; Hoover et al., 2003). Compared to projections from the forelimb and hindlimb representations in SI, the vibrissal-related projections are more numerous and innervate larger parts of the neostriatum. This is consistent with the fact that the whisker representation occupies the largest portion of the somatotopic map in SI.

• Combinatorial maps: Studies that used 2-deoxyglucose to characterize the topography of neostriatal responsiveness to peripheral stimulation revealed regions of maximal activation that formed a basic map of the limbs and trunk (Brown, 1992). Additional patches of secondary activation, however, revealed the juxtaposition of different body part elements in unique combinations. Consistent with corticostriatal divergence, these complex patterns suggest that different neostriatal zones represent the substrate for integrating specific combinations of somatotopic inputs, presumably to mediate specific behaviors or sequences of movements.

• Collateralization: Very few neurons in rat sensorimotor cortex project exclusively to the neostriatum. Instead, corticostriatal projections represent collaterals of axons that also project to the thalamus, globus pallidus, superior colliculus, or other cortical regions (Levesque et al., 1996). This indicates that sensorimotor information sent to the neostriatum is also sent to other brain regions, but the exact function of these projections has not been identified.

Principles of Corticostriatal Convergence

Several principles of corticostriatal convergence have been identified by injecting two anterograde tracers into different pairs of cortical regions and then quantifying tracer overlap in the neostriatum as a function of other features associated with each pair of injections:

• Homology: Homologous functional representations in different cortical areas project to overlapping parts of the neostriatum. As in primates, where the SI and MI hand representations project to overlapping parts of the putamen (Flaherty and Graybiel, 1993), the vibrissal regions in SI, SII, and MI project to overlapping parts of the dorsolateral neostriatum (Alloway et al., 2000; Hoffer and Alloway, 2001). As shown in Fig.<ref>F2</ref>, the MI whisker region projects more rostrally than the projections from SI and SII, yet large parts of the dorsolateral neostriatum receive overlapping projections from each of these cortical areas. In fact, synaptic convergence among SI and MI projections to the dorsolateral neostriatum has been confirmed by electron microscopy (Ramanathan et al., 2002). Furthermore, the whisker regions in SI, SII, and MI are interconnected (Alloway et al., 2004; Chakrabarti and Alloway, 2006; Colechio and Alloway, 2009), and this corroborates the view that interconnected cortical areas often project to overlapping parts of the basal ganglia (Yeterian and Van Hoesen, 1978).

Figure 2: Neostriatal regions that receive the densest projections from whisker-related areas in MI, SI, SII, and the posterior parietal cortex. Distance from bregma is below each section.

• Somatotopic continuity: Corticostriatal projections from SI cortical regions that represent contiguous areas on the same body part (e.g., forepaw and wrist on the forelimb) terminate in overlapping parts of the neostriatum (Hoover et al., 2003). By comparison, projections from SI regions that represent non-contiguous areas (e.g., forepaw and whisker pad) send few overlapping projections to the neostriatum. These distinctions are significant because adjacent subcomponents of the same body part must cooperate with each other during behavioral movements. By contrast, non-contiguous body parts such as the head and arm can move independently of each other. Hence, corticostriatal projections have a topographic organization that enables integration of inputs from cortical regions that must cooperate with each other during behavioral movements.

• Cortical proximity: Cortical sites adjacent to each other project to adjacent parts of the neostriatum. This principle is illustrated by the somatotopic organization of vibrissal maps in the neostriatum, in which neighboring whiskers are represented in neighboring parts of the neostriatum (Wright et al., 1999; Alloway et al., 1999). Furthermore, as shown by Fig.<ref>F3</ref>, the whisker region in the dorsolateral neostriatum has a row-based organization in which projections from each SI barrel row innervate a curved, lamellar-shaped region that lies parallel to the external capsule along the dorsolateral edge of the neostriatum (Brown et al., 1998). Corticostriatal projections from whisker barrel row A terminate most laterally while those from barrel row E terminate most medially (Wright et al., 1999; Alloway et al., 1999).

Figure 3: Topography of afferent whisker projections to SI barrel cortex and the dorsolateral neostriatum. When processed for cytochrome oxidase, tangential sections through layer IV of SI barrel cortex reveal an isomorphic representation of the peripheral whiskers (middle panel). Injections of anterograde tracers into the D5 (red spot) and B2 (blue spot) barrel columns reveal a row-based somatotopic organization in the dorsolateral neostriatum (right panel).

• Anisotropic organization: Consistent with the row-based projection pattern, corticostriatal projections from barrels in the same row overlap more than projections from different rows (Alloway et al., 1999). This anisotropic pattern is noteworthy because barrels in the same row have more interconnections than barrels in different rows. Furthermore, the whiskers move along the rostrocaudal axis, not along the dorsoventral axis. The row-based anisotropic organization of corticostriatal overlap enables integration of inputs from adjacent whiskers that are most likely to contact stimuli in sequential order as the whiskers move back-and-forth during active whisking.

Bilateral corticostriatal projections

Several tracing studies indicate that MI cortex projects bilaterally to the neostriatum (Wilson, 1987; Reiner et al., 2003). More recent analysis, however, indicates that the forepaw region projects most strongly to the ipsilateral neostriatum, whereas the whisker region projects almost equally to the neostriatum on both sides of the brain (Alloway et al., 2009). This is significant because a large fraction of exploratory whisking consists of synchronous whisker movements that are bilaterally symmetric (Mitchison et al., 2007). By comparison, the forepaws are more likely to move independently. These facts suggest that interhemispheric corticostriatal projections from the MI whisker region may represent part of the neuroanatomical substrate for coordinating bilateral whisker movements.

Bilateral corticostriatal projections from the MI whisker region are complemented by interhemispheric projections from other vibrissal-related cortices. As indicated by the schematic diagrams in Fig.<ref>F4</ref>, a small deposit of a retrograde tracer in the dorsolateral neostriatum produces widespread neuronal labeling in the MI, SI, and SII whisker regions of both hemispheres (Alloway et al., 2006). Large numbers of labeled neurons also appear bilaterally in the parietal ventral region and in the posterior parietal cortex. Although neuronal labeling is densest ipsilaterally, the labeling patterns form mirror-image distributions in the sensorimotor regions of both hemispheres. These data demonstrate that the dorsolateral neostriatum processes whisker-related information from multiple regions in both hemispheres, and this supports the view that the vibrissal circuit in the basal ganglia is critical for coordinating bilateral whisker movements.

Figure 4: Bilateral distribution of corticostriatal projections to the dorsolateral neostriatum. A focal deposit of a retrograde tracer (red spot) in the right dorsolateral neostriatum reveals labeled neurons in SI barrel cortex, SII cortex, the parietal ventral region (PV), the posterior parietal cortex (PPC), and the MI whisker region of both hemispheres.

Dorsocentral neostriatum

Although the MI whisker region has strong connections with the dorsolateral neostriatum, most corticostriatal projections from MI terminate more centrally in what is called the dorsocentral neostriatum (Alloway et al., 2009). This is noteworthy because the dorsocentral neostriatum also receives dense projections from the posterior parietal cortex (Reep et al., 2003). Like other pairs of cortical regions that send converging projections to the neostriatum, the MI whisker region and posterior parietal cortex are directly interconnected (Reep et al., 1994; Colechio and Alloway, 2009). The posterior parietal cortex receives vibrissal information from both POm and the adjacent SI barrel cortex, as well as inputs from the auditory and visual cortical areas. These connections suggest that the posterior parietal cortex integrates vibrissal inputs with other sensory modalities that contain spatial information about salient stimuli near the animal’s head. Consistent with this view, behavioral lesion experiments indicate that the posterior parietal cortex is critical for guiding head movements during directed attention (Kesner et al., 1989; Crowne et al., 1992; Tees, 1999). Collectively, these findings suggests that the dorsocentral neostriatum uses whisker-related inputs from MI and the posterior parietal cortex to coordinate whisking with head movements and other orienting behaviors that subserve directed attention (Reep and Corwin, 2009).

Neostriatal computations

Corticostriatal convergence is consistent with prevailing views about the computational functions of the neostriatum. Specifically, medium spiny neurons have distinct biophysical properties that enhance the detection of synchronous inputs. In conjunction with low rates of spontaneous activity, the membrane potentials of medium spiny neurons do not fluctuate randomly, but switch rapidly between “down” (-80 mv) and “up” (-50 mv) states (Kawaguchi et al., 1989). Because medium spiny neurons have strong rectifying potassium currents that shunt small excitatory inputs, these neurons shift to the “up” state and discharge action potentials only when they receive strong excitation. Corticostriatal axons traverse the neostriatal neuropil in a relatively straight path and contribute few synaptic inputs to each of the neostriatal neurons that they contact (Kincaid et al., 1998). Consequently, many convergent corticostriatal terminals must discharge simultaneously to drive a neuronal target to the “up” state (Wilson, 1995). Hence, vibrissal-related neostriatal neurons probably signal when multiple vibrissal regions in the cortex are co-activated during whisking behavior or when the whiskers contact external objects. Interconnections between related cortical areas increase the synchronization of these regions, thereby increasing the probability that their convergent corticostriatal projections will depolarize a postsynaptic target towards the “up” state.

Neostriatal vibrissal responses

Few studies have characterized the responses of neostriatal neurons to vibrissal inputs. Consistent with the fact that corticostriatal neurons use glutamate as an excitatory neurotransmitter (Ottersen and Storm-Mathisen, 1984; Gundersen et al., 1996), electrical stimulation of barrel cortex evokes neuronal activity in the dorsolateral neostriatum of anesthetized animals (Wright et al., 2001). In awake behaving rats, neurons in the dorsolateral neostriatum are excited by passive whisker stimulation or discharge in phase with the rhythmic movements of the whiskers during behavioral exploration (Carelli and West, 1991). In the anesthetized preparation, however, mechanical deflection of the whiskers does not evoke discharges in neostriatal neurons (West, 1998). The fact that neostriatal neurons do not respond to whisker stimulation when the animal is anesthetized is consistent with the view that the sensorimotor channel plays a critical role in the selection and control of internally-generated behavioral movements.

Neostriatal vibrissal functions

No study has specifically examined the behavioral effects produced by selectively disrupting the vibrissal circuits in the basal ganglia. The only data close to addressing this issue come from experiments that characterized the temporal patterns or sequences of stereotyped grooming behaviors (Cromwell and Berridge, 1996). This work indicates that a focal lesion in a specific part of the dorsolateral neostriatum destroys the normal sequence of stereotyped grooming movements, but such lesions do not alter the capacity to emit the grooming movements. Consistent with this, neurons in this part of the dorsolateral neostriatum encode the serial order or chain of sequential grooming movements (Aldridge and Berridge, 1998). The neostriatal site that is crucial for normal grooming sequences is located in a part of the dorsolateral neostriatum that receives projections from the forepaw and whisker representations in SI cortex (Hoover et al., 2003).

These and other studies indicate that the neostriatum is important for linking sequences of well-learned behaviors. Whisking is clearly a well-learned stereotyped behavior that is characterized by sequential epochs in which the frequency of whisker movements is relatively constant in one epoch (1-2 sec), but shifts to another frequency in the next epoch. Some data suggest that central pattern generators in the brainstem maintain whisking frequency within an epoch, but a central pattern generator alone cannot mediate the shift from one frequency to another. Hence, the vibrissal processing region in the dorsolateral neostriatum may coordinate the initiation and sequencing of whisking movements in conjunction with sniffing and other behaviors that involve sequential movements of the head and neck.

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Sponsored by: Prof. Tony J. Prescott, Dept Psychology, Univ of Sheffield, UK

Reviewed by: Anonymous (via Prof. Tony J. Prescott, Dept Psychology, Univ of Sheffield, UK)

Reviewed by: Anonymous (via Dr. Jen Lewis, University of Sheffield, Sheffield, United Kingdom)

Accepted on: 2013-06-03 22:52:18 GMT