Vibrissal midbrain loops
|Manuel Castro-Alamancos and Asaf Keller (2011), Scholarpedia, 6(6):7274.||doi:10.4249/scholarpedia.7274||revision #150425 [link to/cite this article]|
Components of the vibrissa midbrain network: superior colliculus
The midbrain consists of the tectum and the tegmentum. The tectum comprises the inferior colliculus and superior colliculus. The tegmentum contains several areas including the periaqueductal gray, mesencephalic reticular formation (aka, deep mesencephalic nucleus), cuneiform nucleus (also commonly referred in rodents as deep mesencephalic nucleus), laterodorsal tegmental nucleus (LDT), pedunculopontine tegmental nucleus (PPT), red nucleus, substantia nigra and ventral tegmental area. The midbrain also contains ascending and descending fiber bundles such as the cerebral peduncle, the medial lemniscus and the lateral lemniscus. Among these areas, the superior colliculus is well known to receive vibrissal sensory inputs from the trigeminal complex and to project to vibrissa motoneurons in the facial nucleus. Thus, we will focus on the superior colliculus below. Apart from the superior colliculus, it is worth mentioning that the lateral column of the periaqueductal gray (Beitz, 1982) and the mesencephalic reticular formation (Veazey and Severin, 1982) receive some trigeminal afferents. Also, the red nucleus, mesencephalic reticular formation and periaqueductal gray oculomotor nucleus project to vibrissa motoneurons (Hattox et al., 2002). Vibrissa motor cortex projects directly to vibrissa motorneurons (Grinevich et al., 2005) and also indirectly by innervating each of the midbrain regions that project to vibrissa motorneurons (Hattox et al., 2002).
The rat superior colliculus is divided into superficial, intermediate and deep layers. There are three superficial layers (I-III); the zonal layer (stratum zonale), the superficial gray layer (stratum griseum superficiale) and the optic layer (stratum opticum). There are two intermediate layers (IV-V); the intermediate gray layer (stratum griseum intermediale) and the intermediate white layer (stratum album intermediale). There are two deep layers (VI-VII); deep gray layer (stratum griseum profundum) and deep white layer (stratum album profundum). The superficial layers receive dense visual inputs from retina, primary visual cortex and cholinergic inputs from parabigeminal nucleus (PB), and project to deeper layers in the superior colliculus and to the thalamus. The intermediate layers receive direct somatosensory and auditory inputs, as well as inhibitory inputs from the substantia nigra pars reticulata and cholinergic inputs from the PPT and LDT. These sensory modalities become integrated with visual information arriving from the superficial layers, so that visual, auditory and somatosensory maps lie in spatial register across the collicular layers (Drager and Hubel, 1975b; Stein et al., 1975).
Since this article is about vibrissa, we will focus on the intermediate and deep layers (aka, deeper layers). For reviews of the cell types, circuitry and functions of cells in the superficial layers of the superior colliculus the reader is referred to the following references (Stein, 1981; May, 2005). The deeper layers contain mostly multipolar cells of various types located in all layers and horizontal cells, which are GABAergic interneurons. Large multipolar cells whose dendrites cross several layers give rise to predorsal bundle fibers, a main output of the superior colliculus. Intrinsic collicular circuitry distributes excitatory as well as inhibitory collicular activity within and across layers and across major collicular subdivisions (Zhu and Lo, 2000; Meredith and King, 2004; Tardif et al., 2005).
Vibrissal superior colliculus inputs
There are two sources of vibrissa inputs that reach the superior colliculus: a direct input from the trigeminal complex (trigeminotectal) and an indirect input from the barrel cortex (corticotectal). In addition, there are other pathways that may regulate vibrissa inputs (see Figure 1).
- Trigeminotectal pathway: The trigeminal complex projects to the deeper layers of the superior colliculus, particularly the intermediate layers. Trigeminal complex is divided into principal (PrV) and spinal (SpV) nuclear divisions. The spinal nucleus is further divided into three subnuclei: subnucleus interpolaris (SpVi), oralis (SpVo) and caudalis (SpVc). Between 10-30% of PrV cells, which have large multipolar somata with expansive dendritic trees and multiwhisker receptive fields, project to the superior colliculus, and also to POm and zona incerta (ZI) (Killackey and Erzurumlu, 1981; Huerta et al., 1983; Bruce et al., 1987; Rhoades et al., 1989; Veinante and Deschenes, 1999). Likewise, cells in SpVi and SpVo, which have multiwhisker receptive fields, project to the superior colliculus; these cells project also to POm and zona incerta. In contrast, SpVc has few projections to the superior colliculus. Thus, the trigeminotectal pathway is formed by cells with multiwhisker receptive fields located in PrV, SpVi and SpVo.
- Corticotectal pathways: Layer V cells in both the vibrissa motor cortex (Miyashita et al., 1994) and the barrel cortex (Wise and Jones, 1977) project to the deeper layers of the superior colliculus.
- Nigrotectal pathway: GABAergic cells in the ipsilateral substantia nigra pars reticulata project to the deeper layers of the superior colliculus where they directly contact cells that form the predorsal bundle (Harting et al., 1988; Redgrave et al., 1992; Kaneda et al., 2008). There is also a smaller projection from the contralateral substantia nigra pars reticulata, and sensory (visual) inputs have opposing effects on crossed and uncrossed nigrotectal cells (Jiang et al., 2003).
- Incertotectal pathway: GABAergic cells from the zona incerta project to the superior colliculus (Kolmac et al., 1998). Interestingly, zona incerta cells are contacted by trigeminal afferents that provide vibrissa information to the superior colliculus, and posterior thalamus (Lavallee et al., 2005). The superior colliculus also projects to the zona incerta (see below).
- Neuromodulatory pathways: Cholinergic cells from PPT and LDT (Beninato and Spencer, 1986; Krauthamer et al., 1995; Billet et al., 1999), noradrenergic cells from the locus coeruleus (Swanson and Hartman, 1975), and serotoninergic cells from the dorsal raphe nucleus (Steinbusch, 1981; Beitz et al., 1986) project to the superior colliculus.
Vibrissal superior colliculus outputs
The main efferents of the superior colliculus can be divided into ascending and descending projections (see Figure 1).
Ascending output pathways
- Tectothalamic pathways: A large number of thalamic nuclei are contacted by the superior colliculus, including nuclei in the posterior, lateral, geniculate, intralaminar and midline groups (Roger and Cadusseau, 1984; Yamasaki et al., 1986; Linke et al., 1999; Krout et al., 2001). The rostral sector of the posterior nucleus of the thalamus (POm), which is driven by whisker stimulation, also receives afferents from the superior colliculus (Roger and Cadusseau, 1984). In turn, POm projects to the barrel cortex providing a loop back to the superior colliculus via corticotectal pathways. The other major superior colliculus projections to the thalamus reach the intralaminar nuclei (i.e. particularly the parafascicularis nucleus, followed by central lateral, paracentral and central medial) and midline nuclei (Yamasaki et al., 1986; Grunwerg and Krauthamer, 1990; Krout et al., 2001). In turn, cells in the intralaminar nuclei project to the striatum, giving rise to a loop through the basal ganglia back to the superior colliculus (McHaffie et al., 2005).
- Tectoincertal pathway: The superior colliculus projects to the zona incerta (Kolmac et al., 1998) and dorsal aspect of the nucleus reticularis of the thalamus (nRt) (Kolmac and Mitrofanis, 1998). The tectoincertal pathway targets a different part of the zona incerta (dorsal) than the origin of the incertotectal pathway (ventral). The GABAergic cells in nRt and zona incerta are well known to modulate vibrissal responses in dorsal thalamus (Trageser and Keller, 2004; Hirata et al., 2006).
- Tectonigral pathway: The superior colliculus projects to dopaminergic cells in the substantia nigra pars compacta (Coizet et al., 2003; Comoli et al., 2003; Coizet et al., 2007). Interestingly, through this pathway sensory stimuli may be identified as unpredicted and salient (Redgrave and Gurney, 2006). The superior colliculus also projects to the subthalamic nucleus in the basal ganglia (Coizet et al., 2009).
- Pretectal pathways: The superior colliculus provides an extensive terminal field to the nucleus of the optic tract and the posterior pretectal nucleus, mainly from the superficial layers. In turn, the pretectum provides feedback connections back to the superior colliculus (Taylor et al., 1986).
- Tectotectal commissural pathway: This pathway originates in the deeper layers and connects the two superior colliculi on both sides of the brain (Sahibzada et al., 1987). These fibers may mediate mutually suppressive effects on the output of the contralateral colliculus to control competing responses (Sprague, 1966).
Descending output pathways
The main descending output pathways that originate in separate subregions of the deeper layers and mediate approach and escape responses (Redgrave et al., 1987a, b; Dean et al., 1989; Westby et al., 1990; Redgrave et al., 1993) are:
- Predorsal bundle pathways: This is a crossed descending projection that contacts targets in the contralateral brainstem, including precerebellar nuclei (e.g. reticularis tegmenti pontis, inferior olive), and spinal cord. Approach responses toward salient stimuli are mediated by this pathway. In addition, many of the cells that give rise to this pathway (>50%) are driven by whisker stimulation (Westby et al., 1990).
- Ipsilateral efferent bundle pathways: This is an ipsilateral descending projection with terminations in the periaqueductal gray, cuneiform nucleus, lateral pons and ventral pontine/medullary reticular formation. Escape behaviors rely on this ipsilateral efferent pathway. Few cells (~14%) that give rise to this pathway respond to whisker stimulation (Westby et al., 1990).
Superior colliculus activity driven by passive touch
Several studies have described whisker evoked responses in the superior colliculus of the rat (Stein and Dixon, 1979; Fujikado et al., 1981; McHaffie et al., 1989; Grunwerg and Krauthamer, 1990; Cohen and Castro-Alamancos, 2007; Hemelt and Keller, 2007; Cohen et al., 2008), mouse (Drager and Hubel, 1975a) and hamster (Chalupa and Rhoades, 1977; Finlay et al., 1978; Stein and Dixon, 1979; Rhoades et al., 1983; Larson et al., 1987; Rhoades et al., 1987). Together these studies indicate that whisker-sensitive superior colliculus cells are rapidly adapting cells with large receptive fields and display angular selectivity.
Although superior colliculus cells respond relatively effectively to single whiskers, including the principal whisker (PW) and several adjacent whiskers (AWs), cells respond much more robustly to simultaneous, or nearly simultaneous, wide-field (multiwhisker) stimuli (Cohen et al., 2008) (see Figure 2). The enhanced multiwhisker response is temporally stereotyped, consisting of two short latency excitatory peaks (peak1 and peak2) separated by ~10 ms that have different characteristics and origins. These properties make superior colliculus cells highly sensitive to the degree of temporal dispersion of stimulated whiskers during multiwhisker stimulation. The spikes evoked during peak1 show very little jitter and are driven by direct trigeminotectal excitatory postsynaptic potentials (EPSPs) from different single whiskers that sum to produce a robust multiwhisker response. The spikes evoked during peak2 are much more dispersed and are driven by EPSPs returning to the superior colliculus from the barrel cortex that ride on top of an evoked inhibitory postsynaptic potential (IPSP). Consistent with their cortical origin, peak2 responses are highly dependent on the level of forebrain activation. These properties make superior colliculus cells highly sensitive to the order and temporal dispersion of multiwhisker stimulation. Cells are most responsive when the PW is stimulated first and AWs follow at short intervals between 0-10 ms. However, when the AWs are stimulated first and with an interval above 2 ms, the cells do not respond at all to the PW and this suppression starts to recover at intervals above 50 ms (Cohen et al., 2008).
Populations of superior colliculus cells are tuned to respond robustly when their PW contacts an object first and other whiskers follow within <10 ms, and to remain silent when their PW contacts an object >2 ms after other whiskers. These response characteristics are likely useful to signal contact with an object as rats navigate the environment because a selective population of superior colliculus cells representing the first contacted whiskers will discharge. This may well serve as a signal to orient toward the contact location, which (as discussed below) is a putative function of the superior colliculus.
Superior colliculus activity driven by whisking movement, active touch and texture
Rats sense the environment through rhythmic vibrissa protractions, called active whisking, which can be simulated in anesthetized rats by electrically stimulating the facial motor nerve (Zucker and Welker, 1969; Szwed et al., 2003). Simultaneous recordings from the barrel cortex and superior colliculus have shown that, similar to passive touch, whisking movement is signaled during the onset of the whisker protraction by short-latency responses in barrel cortex that drive corticotectal responses in superior colliculus, and all these responses show robust adaptation with increases in whisking frequency (Bezdudnaya and Castro-Alamancos, 2011). Active touch and texture are signaled by longer latency responses, first in superior colliculus during the rising phase of the protraction, likely driven by trigeminotectal inputs, and later in barrel cortex by the falling phase of the protraction. Thus, superior colliculus can decode whisking movement, active touch and texture.
Vibrissa movements driven by superior colliculus
The superior colliculus sends dense and direct projections to the rat facial nucleus, where the vibrissa motor neurons are located (Miyashita and Mori, 1995; Hattox et al., 2002), and stimulation of the superior colliculus produces movements of the vibrissae (McHaffie and Stein, 1982; Hemelt and Keller, 2008). Microstimulation throughout the deeper layers of the superior colliculus produces sustained ipsilateral (ventral sites), contralateral (dorsal sites) or bilateral (intermediate sites) vibrissa protractions, frequently outlasting the stimulus duration (see movie clip at http://jn.physiology.org/content/100/3/1245/suppl/DC1). Thus, the deeper layers appear to preferentially target the ipsilateral efferent bundle drive, while more superficial layers target the contralateral predorsal bundle. In addition, tecto-facial neurons rarely (9%) receive direct trigeminal inputs, so that the colliculus does not seem to act as a simple closed sensorimotor loop (Hemelt and Keller, 2008).
The movements elicited by stimulating the superior colliculus are very different from the rhythmic movements evoked by identical stimulation in the motor cortex (Hemelt and Keller, 2008). For instance, the motor cortex evokes rhythmic protractions that are much smaller than the sustained protractions produced by superior colliculus. In addition, superior colliculus evoked movements have much shorter latencies than those evoked from the motor cortex (8 ms vs. >30 ms). Motor cortex appears to regulate whisking frequency, acting through a brain stem central patter generator, while the superior colliculus may be controlling the amplitude and set point of whisking.
Behavioral state and neuromodulator influences in superior colliculus
The spontaneous firing of vibrissa-sensitive cells in the superior colliculus is dependent on the behavioral state of the animal (see Figure 3). Firing is much higher during active exploration, which includes active whisking, and paradoxical or rapid eye movement sleep (REM) compared to awake immobility and slow wave sleep. Thus, according to firing rate, the superior colliculus is activated during active exploration and REM sleep, and deactivated during awake immobility and slow wave sleep (Cohen and Castro-Alamancos, 2010b). The superior colliculus appears to come online during active exploratory states and rapidly goes offline during awake immobile periods. Particularly interesting are periods during awake immobility when superior colliculus firing ceases completely (Cohen and Castro-Alamancos, 2010b).
Firing in superior colliculus is not eliminated during sleep. During slow wave sleep, firing seems to be driven by slow oscillations in neocortex via the corticotectal pathway. This is expected because corticotectal influence is strongest during the deactivated mode (Cohen et al., 2008). The driver for REM related activity is not known, but cannot be movement or sensory input such as during active exploration. One possibility is that superior colliculus during REM is driven by the actions of specific neuromodulator systems. For example, activity in cholinergic brainstem nuclei is significant during REM sleep (el Mansari et al., 1989), these nuclei innervate the superior colliculus (Beninato and Spencer, 1986; Krauthamer et al., 1995; Billet et al., 1999), and acetylcholine activates some superior colliculus neurons in vitro (Li et al., 2004; Sooksawate and Isa, 2006). Thus, cholinergic activation likely causes enhanced spontaneous firing during REM sleep.
Sensory responses in superior colliculus are also dependent on behavioral state. In particular, corticotectal responses (peak2) evoked by whisker stimuli are larger during the deactivated mode than during the activated mode, just like the cortical responses on which they depend (Cohen et al., 2008; Cohen and Castro-Alamancos, 2010b). However, longer latency responses (peak3; of unknown origin) are typically larger during the activated mode. Sensory responses that are driven by different neural circuits are regulated differently by behavioral state. The stronger corticotectal responses of whisker-sensitive cells in the intermediate layers of the superior colliculus during deactivated modes may be useful as a powerful alerting stimulus in an animal that is sleeping, drowsy, or inattentive, and an unknown moving object or animal makes contact with its whiskers. Interestingly, superior colliculus responses evoked by air-puff stimuli are largest when the animal is quiescent and orients to the stimulus (Cohen and Castro-Alamancos, 2010b).
As already mentioned, neuromodulators are likely to drive the spontaneous firing and sensory response changes related to specific states. Although, cholinergic, noradrenergic and 5-HT neurons project to the superior colliculus, the effects of these neuromodulators on vibrissa-sensitive superior colliculus cells are unknown.
Functional role of superior colliculus vibrissa networks
The superior colliculus is an early sensory hub well suited to mediate sensory detection of stimuli that require immediate action (Sprague and Meikle, 1965; Schneider, 1969; Sparks, 1986; Dean et al., 1989; Westby et al., 1990; Redgrave et al., 1993; Stein and Meredith, 1993; McHaffie et al., 2005; Redgrave and Gurney, 2006; Cohen and Castro-Alamancos, 2007). Considering an evolution perspective, in lower vertebrates without significant cortical organization (e.g. amphibians) the superior colliculus acts like the highest brain center controlling escape and approach. With the evolution of neocortex these and more complex functions incorporated the neocortex but the superior colliculus still retains many of these ancient functions. Below we discuss how the superior colliculus basic functions may be relevant to the vibrissal system.
Detect sensory stimuli
As discussed above, cells in the superior colliculus are highly sensitive to passive and active touch. In behaving animals, the trigeminotectal sensory pathway is capable of independently (i.e. in the absence of thalamocortical networks) detecting relevant (i.e. that signal impending danger) sensory stimuli applied to the whisker pad as long as the stimulus is sufficiently salient (Cohen and Castro-Alamancos, 2007). However, the trigeminotectal pathway must work in synergy with thalamocortical networks to detect stimuli of low saliency (Cohen and Castro-Alamancos, 2010a). Low intensity stimuli may not be detectable by the superior colliculus alone because the neural responses they evoke are weak and dispersed, and this sparse code is further suppressed when corticotectal inputs driven by the stimulus are absent (i.e. during thalamocortical inactivation) (Cohen et al., 2008). Therefore, the superior colliculus may require corticotectal inputs driven by the sensory stimulus to enhance direct trigeminotectal sensory responses for successful detection of low salience stimuli.
Whisker sensitive cells in the intermediate layers of the superior colliculus respond most effectively to multiwhisker stimuli when the PW is stimulated first and other whiskers follow shortly within 10-ms (Cohen et al., 2008). This means that only the cells representing the first stimulated whiskers will fire and the cells representing the succeeding whiskers will be inhibited. Such an arrangement suggests a population code signaling the whiskers that first made contact. This is likely very useful during navigation and exploration in order to detect the presence of objects.
Gate orienting responses to detected sensory stimuli depending on the state of the animal and the significance of the stimulus
After detection of initial contact with a salient stimulus, a primary function of the whisker sensitive cells in the intermediate layers of the superior colliculus may be to gate the induction of appropriate orienting responses depending on the level of alertness of the animal. If the animal is already alert, an initial contact does not usually elicit a strong orienting response. However, if the animal is quiescent or inattentive, an initial contact with a salient stimulus usually elicits strong orienting. The superior colliculus is well known to be involved in orienting responses to innocuous and painful stimuli from a wide range of modalities, including somatosensory, auditory and visual (Sprague and Meikle, 1965; Wurtz and Albano, 1980; Meredith and Stein, 1985; Sparks, 1986; Dean et al., 1989; Stein and Meredith, 1993; Stein, 1998).
As already mentioned, whisker sensitive cells in the intermediate layers elicit highly stereotyped peak1 and peak2 responses in close succession when stimulated by salient stimuli, such as near-simultaneous multiwhisker stimulation. The occurrence of successive spikes separated by short intervals has strong impact on the target neurons due to temporal synaptic summation. The interesting aspect of the superior colliculus response is that the first and successive spikes are independently regulated. In particular, peak2 depends on cortical feedback which is strongly regulated by behavioral state (Castro-Alamancos, 2004a, b). The strongest output of whisker sensitive cells in the intermediate layers of the superior colliculus occurs for nearly simultaneous multiwhisker contacts during quiescent states (Cohen et al., 2008; Cohen and Castro-Alamancos, 2010b). This is likely useful as a powerful alerting stimulus in an animal that is sleeping, drowsy or inattentive, and an unknown moving object or animal makes contact with its whiskers. Since the target of these cells in deeper layers and in the brainstem drive orienting responses (Redgrave et al., 1987a; Dean et al., 1989; Westby et al., 1990), such a powerful alerting output makes good functional sense. The two main types of behaviors gated by the superior colliculus are to:
- Approach (move toward) sensory stimuli: Orienting motor behaviors elicited by the superior colliculus occur via the crossed descending projections from the deeper layers (Redgrave et al., 1987a; Dean et al., 1989; Westby et al., 1990; Redgrave et al., 1993). Moreover, the ability of the superior colliculus to control the direction and speed of eye (McHaffie and Stein, 1982), head (Dean et al., 1986), and whisker movements (Hemelt and Keller, 2008) is particularly germane in this orienting role. Whisker-responsive cells in the intermediate layers of the superior colliculus are associated with the contralaterally projecting predorsal bundle (Westby et al., 1990), which mediates approach movements towards novel stimuli (i.e. orienting responses) (Dean et al., 1989). Enhancement of sensory responsiveness through this pathway during orienting responses makes functional sense; the stronger neural activity during overt orienting responses may well reflect the neural drive for the orienting responses (Cohen and Castro-Alamancos, 2010b).
- Escape (move away) sensory stimuli: Stimulation of the superior colliculus produces defensive behaviors, such as escape responses (Bandler et al., 1985; Dean et al., 1988; Dean et al., 1989; Brandao et al., 1994; Brandao et al., 2003). Cells in deeper layers also respond to noxious stimuli (Stein and Dixon, 1979; McHaffie et al., 1989; Redgrave et al., 1996a) and certain nocifensive reactions depend on the integrity of the superior colliculus (Redgrave et al., 1996b; Wang and Redgrave, 1997; McHaffie et al., 2002). Interestingly, whisker and nociceptive face inputs converge in the superior colliculus and may control face orientation and withdrawal responses during active whisking exploration (McHaffie et al., 1989), which is critical for navigation in rodents. Escape responses elicited by fear also involve the superior colliculus (Cohen and Castro-Alamancos, 2007, 2010a, c); rats use the superior colliculus to detect a whisker pad stimulus that elicits fear because of its association with an aversive event. In essence, the superior colliculus is a site where sensory inputs can directly control behavior, directing the animal towards objects of interest and away from objects that might pose a threat.
Activate (wake-up) the forebrain in response to sensory stimuli
The superior colliculus responses driven by sensory stimulation may also serve to trigger forebrain activation in quiescent animals by impacting on neuromodulatory systems in the midbrain and brainstem that cause cortical activation (Castro-Alamancos, 2004b). These neuromodulatory nuclei are well known targets of superior colliculus cells (Redgrave et al., 1987b; Dean et al., 1989; Redgrave et al., 1993).
In summary, whisker-sensitive cells in the intermediate layers are excellent detectors of initial whisker contact, and their output (i.e. the ability to drive target cells) is independently regulated by converging trigeminal synaptic inputs and cortical feedback. Because spikes driven by cortical feedback are gated by behavioral state, they provide a powerful mechanism for driving target cells depending on the level of arousal. This mechanism may serve to gate orienting responses and forebrain activation in quiescent animals. The main role of the superior colliculus may be to detect novel or salient sensory stimuli and to elicit an appropriate response to it (approach, ignore or escape). The superior colliculus can serve as an early relay station for rapid detection of sensory signals that have gained behavioral significance through learning and that call for immediate action.
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