Vibrissal basal ganglia circuits
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 and thalamus. While most of this information comes from the vibrissal regions in the primary somatosensory (SI) and motor (MI) cortical areas, some whisker information is transmitted much more rapidly to the basal ganglia by intralaminar and other thalamic nuclei. A series of interconnected nuclei in the basal ganglia transform these whisker-related inputs, and the processed output is then sent to other thalamic nuclei that project to several cortical areas. Although the vibrissal circuits in the basal ganglia are poorly understood, many findings support the view that these circuits are involved in regulating the 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) actively move their whiskers to acquire tactile information about the spatial features of external objects (Rice, 1995). In other species with vibrissae (e.g., rabbit, cat, dog, squirrel, chipmunk), tactile information is acquired from passive whisker stimulation that occurs as the animal moves through space or as objects move past the animal’s head. Although the basal ganglia process tactile information produced by passive whisker stimulation, scientific interest in using the whisker system to understand the functional mechanisms of the basal ganglia has focused on the active whisking system of rats and mice.
Vibrissal basal ganglia connections
The vibrissal circuit extends across the same set of interconnected nuclei as in other basal ganglia channels. Consistent with this scheme, the striatum receives inputs from sensorimotor cortical areas that are specialized for processing sensory information received from the peripheral whiskers. Corticostriatal projections originate from cortical layers III and V (Reiner et al., 2003), use glutamate as an excitatory neurotransmitter (Ottersen and Storm-Mathisen, 1984; Gundersen et al., 1996), and terminate largely on medium spiny neurons in the striatum, which use GABA as an inhibitory neurotransmitter (Kincaid et al., 1998). Medium spiny neurons represent the source of all efferent projections from the striatum, and axons from these neurons project to the entopeduncular nucleus, the pars reticulata of the substantia nigra, and to the lateral globus pallidus. All of these striatal nuclei use GABA as an inhibitory neurotransmitter, and the projections from the entopeduncular nucleus and the substantia nigra pars reticulata project to motor- related nuclei in the thalamus, especially the ventromedial and ventrolateral nuclei, which project to sensorimotor cortex.
Vibrissal cortical areas
In rats and mice, whisker-related sensory information is transmitted to SI cortex by two parallel pathways that originate in the brainstem and proceed to the contralateral thalamus. The lemniscal trigeminal pathway originates from the principal sensory trigeminal (PrV) nucleus and terminates in the ventromedial (VPM) thalamus. The paralemniscal trigeminal pathway originates from the interpolaris division of the spinal trigeminal (SPVi) nucleus and terminates in the medial part of the posterior (POm) thalamus. The thalamic nuclei for both of these pathways convey information to the SI barrel field, which represents the main cortical area for processing vibrissal information (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 sends dense projections to the layer IV septa that separate individual barrels from each other.
As seen in Figure 1, several cortical areas receive vibrissal-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 (Cavell and Simons, 1987; Spreafico et al., 1987; Fabri and Burton, 1991). In addition, the parietal ventral cortex (PVC) receives dense projections from SI barrel cortex (Fabri and Burton, 1991), and the posterior parietal cortex (PPC) receives projections from SI barrel cortex and POm, but not from VPM (Reep et al., 1994; Lee et al., 2011). All of these cortical areas, including SI barrel cortex, convey vibrissal information to the basal ganglia.
The MI whisker region also processes vibrissal-related information and conveys it to the striatum. While the MI whisker region is operationally defined by sites in which intracranial microstimulation evokes whisker twitches (Gioanni and Lamarche, 1985; Brecht et al., 2004), extracellular recordings demonstrate that mechanical deflections of the whiskers can activate neurons in the deep layers of MI, but not if somatosensory cortex has been inactivated (Chakrabarti et al., 2008). Therefore, even though POm sends some projections directly to MI (Aldes, 1998; Alloway et al., 2004; Colechio and Alloway, 2009), the functional impact of whisker stimulation on MI is mediated mainly by its cortical inputs from SI and SII.
Vibrissal corticostriatal projections
The vibrissal circuit undoubtedly extends through all basal ganglia nuclei, but most studies of this sensorimotor channel have focused on the striatum, especially its dorsolateral region. Like other striatal regions, the dorsolateral part receives dopaminergic inputs from the substantia nigra pars compacta, as well as glutamatergic inputs from the thalamic intralaminar nuclei. Whisker-related regions in the dorsolateral striatum also receive dense thalamic inputs from POm (Smith et al., 2012), which represents part of the ascending paralemniscal trigeminal pathway.
As shown in Figure 2, the dorsolateral striatum receives whisker related sensory inputs from multiple cortical areas including SI barrel cortex, SII, and PPC (Levesque et al., 1996b; Brown et al., 1998; Alloway et al., 2006; Smith et al., 2012). The MI whisker region, which is located in medial agranular cortex (Brecht et al., 2004), projects to the striatum and innervates the dorsolateral and dorsocentral regions (Hoffer and Alloway, 2001; Reep et al., 2003). Quantitative analysis of the projections from SI, MI, and other cortical areas has revealed several principles of corticostriatal organization in the vibrissal and related sensorimotor circuits:
- Somatotopic organization: Projections from the head, limb, and trunk representations in SI cortex terminate in distinct, yet overlapping, parts of the striatum. Consequently, the striatum contains a crude somatotopic map in which the forepaw region is located ventral to the hindpaw region, and both limb representations are medial and rostral to the main part of the vibrissal representation (Carelli and West, 1991; Brown, 1992; Hoover et al., 2003). Compared to the forelimb and hindlimb projections, the vibrissal- related projections are more numerous and innervate larger parts of the striatum. This is consistent with the fact that the whisker representation occupies the largest portion of the SI somatotopic map.
- Divergence: In both rodents and primates, corticostriatal projections in the sensorimotor channel have a one-to-many projection pattern (Flaherty and Graybiel, 1991). In the vibrissal system, projections from individual whisker-barrel columns in SI terminate in multiple, discontinuous patches in the dorsolateral striatum (Alloway et al., 1998). Divergent corticostriatal projections represent a mechanism for distributing the same sensorimotor information to multiple processing zones in the striatum.
- Convergence: Complementing this one-to-many projection pattern, each striatal region receives overlapping inputs from several cortical sites. An early primate study 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 characterized by large amounts of corticostriatal overlap (Alloway et al., 1999, 2000; Hoffer and Alloway, 2001).
- Combinatorial maps: Experiments using 2-deoxyglucose to reveal striatal regions that are maximal activated during tactile stimulation indicate that elements of different body parts are represented in multiple locations that are juxtaposed in unique combinations (Brown, 1992). Consistent with both divergent and convergent projections, these complex patterns suggest that different striatal zones represent the substrate for integrating specific combinations of somatotopic inputs, presumably to mediate specific behaviors or sequences of movements.
- Collateralization: Few neurons in rat sensorimotor cortex project exclusively to the striatum. Instead, corticostriatal projections represent collaterals of axons that project to the thalamus, globus pallidus, subthalamic nucleus, superior colliculus, and certain cortical regions (Levesque et al., 1996a). This indicates that sensorimotor information sent to the striatum 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 different anterograde tracers into separate cortical sites of the same animal and then quantifying the amount of tracer overlap in the striatum as a function of the features associated with each pair of injections:
- Homology: Homologous functional representations in different cortical areas project to overlapping parts of the striatum. Like primates, in which 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 adjacent and overlapping parts of the striatum as shown in Figure 2(Alloway et al 2000; Hoffer and Alloway, 2001). Consistent with these projection patterns, electron microscopy confirms that individual striatal neurons often receive convergent synaptic inputs from whisker regions in both SI and MI (Ramanathan et al., 2002). The whisker regions in SI, SII, and MI are interconnected (Alloway et al., 2004; Chakrabarti and Alloway 2006; Colechio and Alloway, 2009), and this adds further support to the view that interconnected cortical areas often project to overlapping parts of the basal ganglia (Yeterian and Van Hoesen, 1978).
- Somatotopic continuity: Adjacent SI cortical regions representing contiguous somatic areas (e.g., forepaw and wrist) project to overlapping parts of the striatum (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 striatum. These distinctions are significant because contiguous body parts 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 cooperate with each other during behavioral movements.
- Anisotropic organization: As shown by Figure 3, the whisker region in the dorsolateral striatum has a row- based organization in which corticostriatal projections from each SI barrel row innervate a curved, lamellar- shaped region along the dorsolateral edge of the striatum (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).
This anisotropic pattern is noteworthy because exploratory whisking is characterized by whisker motion along the rostrocaudal axis, not along the dorsoventral axis. Furthermore, barrels in the same row have more reciprocal interconnections than barrels in different rows. Consistent with this row-based organization, corticostriatal projections from the same row overlap more than projections from different barrel rows (Alloway et al., 1999). Hence, the row-like organization of corticostriatal overlap enables greater integration of inputs from the SI barrel columns that are most likely to interact and be coordinated during whisking behavior.
Bilateral corticostriatal projections
The striatum receives MI inputs from both hemispheres (Wilson, 1987; Reiner et al., 2003), but most of these bilateral projections originate from the MI whisker region, not the MI forepaw region (Alloway et al., 2009). This is significant because most exploratory whisking consists of synchronous whisker movements that are bilaterally symmetric (Mitchison et al., 2007). By comparison, the forepaws are much more likely to move independently. These facts suggest that interhemispheric corticostriatal projections from the MI whisker region represent an important 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 Figure 4, a small deposit of a retrograde tracer in the dorsolateral striatum produces neuronal labeling in MI, SI, and SII of both hemispheres (Alloway et al., 2006). Large numbers of neurons also appear bilaterally in the PVC and PPC regions. Cortical labeling is densest ipsilaterally, and the labeling patterns form mirror-image distributions in the sensorimotor regions of both hemispheres. These data demonstrate that the dorsolateral striatum processes whisker-related information from multiple regions in both hemispheres, and this supports the view that the vibrissal basal ganglia circuits help coordinate bilateral whisker movements.
The MI whisker region sends dense projections to the dorsolateral striatum, but most of its corticostriatal projections terminate in the dorsocentral striatum (Alloway et al., 2009), which receives dense projections from the PPC (Reep et al., 2003). Like many other cortical regions that project to overlapping parts of the striatum, the MI whisker region and PPC are interconnected (Reep et al., 1994; Colechio and Alloway, 2009). The PPC 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 PPC integrates vibrissal inputs with other sensory modalities that contain information about salient stimuli near the animal’s head. This view is supported by behavioral lesion studies showing that PPC is critical for guiding head movements during directed attention (Kesner et al., 1989; Crowne et al., 1992; Tees, 1999). Collectively, these findings suggest that the dorsocentral striatum uses whisker-related inputs from MI and the PPC to coordinate whisking with head movements and other orienting behaviors that subserve directed attention (Reep and Corwin, 2009).
Corticostriatal convergence is consistent with prevailing views about the computational functions of the striatum. Medium spiny neurons have strong rectifying potassium currents that shunt small excitatory inputs, but they shift to a depolarized state when they receive strong excitation. Corticostriatal axons traverse the striatal neuropil in a relatively straight path and individual axons contribute only a few synaptic inputs to each striatal neuron that is contacted (Kincaid et al., 1998). Consequently, convergent corticostriatal terminals must discharge simultaneously to drive a striatal neuronal target to its discharge threshold (Wilson, 1995). Hence, whisker-sensitive striatal neurons probably signal when multiple regions in cortex are synchronously active during whisking behavior. Interconnections between the whisker representations in SI, MI, and other sensorimotor cortical areas may increase the synchronization of these regions, thereby increasing the probability that convergent corticostriatal projections will depolarize medium spiny neurons sufficiently to elicit striatal activity during whisking behavior.
Striatal behavioral responses
Substantial evidence indicates that the dorsolateral striatum is needed to execute sensorimotor habits (Yin et al., 2004, 2006; Redgrave et al., 2010). Such behaviors are highly repetitive, are mediated by stimulus-response (S-R) associations, and are expressed even in the absence of reinforcement. In rats, focal lesions in the dorsolateral striatum disrupt the normal sequence of repetitive, stereotyped grooming behaviors [Cromwell and Berridge, 1996). Although the normal sequence of grooming behavior is clearly disrupted, the capacity to emit individual grooming movements is not affected. Consistent with this distinction, neurons in the dorsolateral striatum appear to encode the serial order of sequential grooming movements (Aldridge and Berridge, 1998). Furthermore, the striatal sites associated with stereotyped grooming behaviors are located in regions that receive corticostriatal projections from the forepaw and, to a lesser extent, the whisker representations in SI cortex (Hoover et al., 2003).
In rats, exploratory whisking is a stereotyped behavior that is characterized by a series of short (1-2 sec) whisking bouts or epochs in which the frequency of whisker motion is relatively constant in each epoch, but shifts to another frequency in the next epoch. When whiskers contact external stimuli during exploratory behavior, the whisking behavior is characterized by stereotyped changes in the bilateral pattern of the rhythmic movements (Mitchinson et al., 2007). These stimulus-induced changes appear to reflect the motor expression of an S-R association. These observations suggest that vibrissal processing in the dorsolateral striatum is responsible for coordinating the sequences of whisker movements that accompany exploratory behaviors, including changes in patterns that are evoked by external stimuli. According to this view, corticostriatal projections to the dorsolateral striatum convey sensorimotor signals that accompany the execution of well-learned, habitual behaviors that are performed automatically.
Rodent whisking behavior has many hallmarks of a sensorimotor habit, but very few studies have characterized how dorsolateral striatal neurons respond to vibrissal inputs. Electrical stimulation of SI barrel cortex evokes neuronal discharges in the dorsolateral striatum of anesthetized rats (Wright et al., 2001). In awake rats, neurons in the dorsolateral striatum are excited by passive whisker deflections and discharge rhythmically when rats are actively whisking (Carelli and West, 1991).Whisker deflections rarely evoke striatal discharges in deeply anesthetized rat preparations (West, 1998; Pidoux et al., 2011), but whisker stimulation can reliably evoke neuronal responses in the dorsolateral striatum of rats that are in a lightly anesthetized state (Mowery et al., 2011). As seen in Figure 5, neurons in the dorsolateral striatum display very little adaptation when the whiskers are repetitively deflected at frequencies up to 8 Hz. When neurons in SI barrel cortex and the dorsolateral striatum are recorded simultaneously, SI neurons display quickly adapt to repetitive whisker movements and usually discharge only after neurons in the dorsolateral striatum have already responded.
These facts suggest that striatal responses to passive or external whisker stimulation do not depend on SI inputs. Furthermore, the relative lack of neuronal adaptation in the striatum suggests that invariant neuronal responses may represent the neural mechanism by which the dorsolateral striatum encodes S-R associations that mediate sensorimotor habits. Consistent with this view, whisker-sensitive regions in the dorsolateral striatum receive inputs from several thalamic nuclei that respond to whisker stimulation including the POm and parafascicular (Pf) nuclei (Smith et al., 2012). Although Pf does not receive whisker- related inputs directly from the trigeminal nuclei in the brainstem, it does receive inputs from whisker- sensitive regions in the intermediate layers of the superior colliculus (Smith and Alloway, unpublished observations). In addition, tracer injections into whisker-sensitive regions in the Pf nucleus have revealed projections to both the dorsocentral and dorsolateral striatum.
The superior colliculus is well-known for processing multimodal inputs to enable orientation to salient sensory stimuli (Hemelt and Keller, 2007; Schulz et al., 2009). By receiving direct inputs from the superior colliculus, the Pf nucleus and its projections to the striatum could represent a rapid pre-attentive mechanism that enables highly salient signals to initiate an abrupt change in sensorimotor behavior. Together, the Pf and POm are likely to transmit whisker-sensitive and other somesthetic inputs to the striatum that play an important role in mediating the S-R associations that subserve sensorimotor habits.
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