Single Neuron Studies

1. Topographic Register of Sensory and Motor Representations

Regardless of their origin, the visual, auditory, and somatosensory inputs that reach the SC are arranged systematically to form topographic, or map-like, representations. These sensory maps, like those found in other areas of the brain, are based on the organization of receptive fields (Fig. 3). A neuron's receptive field defines that region of space from which it can be activated by a sensory stimulus, and the arrangement of neurons in the SC is such that adjacent neurons have their receptive fields in adjacent regions of space. When one speaks of a topographic or map-like representation, a frame of reference is always implied, if not stated explicitly. For example, in primary visual structures, the position of a neuron's receptive field is indexed relative to the fovea, which defines the center point of the axes of''visual space.'' Similarly, the receptive field of a neuron in a primary auditory structure would be referred to the center of the head, and in the case of a somatosensory neuron the referent would be the body surface (e.g., face, hand, and leg). One could write volumes about how a topographic representation is an efficient way to encode information about the nature of objects as defined by the spatial relationships of their components (e.g., size, shape,

Figure 3 Visual, auditory, and somatosensory receptive fields are organized in map-like fashion in the superior colliculus (SC) and all share the same axes. The overlapping nature of these representations is particularly evident in individual multisensory neurons. Shown here at the center is a schematic of the left SC as viewed from the top of the brain. Rostral aspects of the SC contain receptive fields that are found in frontal space, caudal locations contain receptive fields in temporal or caudal space, etc. (see text for further detail). The curved line running from the rostral to the caudal SC is the horizontal meridian, which divides the representation of superior from the representation of inferior sensory space. Similarly, the curved line running from medial to lateral represents the vertical meridian, which divides ipsilateral and contralateral sensory space. Representative receptive fields (shading) for multisensory neurons from cat (left) and monkey (right) SC are drawn from rostral (top) and caudal (bottom) sites in the SC. Each concentric circle in the schematics of visual and auditory space represents 10°. In the representation of auditory space, the caudal half of contralateral space is shown by the split hemisphere that has been folded forward. Note the register among the receptive fields for visual-somatosensory and visual-auditory neurons. Visual receptive fields in nasal (frontal) space on the right are linked to somatosensory and auditory receptive fields in frontal space on the right. Similarly, temporal (or caudal) receptive fields in one modality are linked to similar locations in other modalities. Multisensory neurons are found in the deep layers of the SC. These layers are illustrated on a schematic of a coronal (vertical) section through the structure. S, superior; I, inferior; T, temporal; N, nasal; SZ, stratum zonale; SGS, stratum griseum superficiale; SO, stratum opticum; SGI, stratum griseum intermediale; SAI, stratum album intermediale; SGP, stratum griseum profundum; SAP, stratum album profundum.

Figure 3 Visual, auditory, and somatosensory receptive fields are organized in map-like fashion in the superior colliculus (SC) and all share the same axes. The overlapping nature of these representations is particularly evident in individual multisensory neurons. Shown here at the center is a schematic of the left SC as viewed from the top of the brain. Rostral aspects of the SC contain receptive fields that are found in frontal space, caudal locations contain receptive fields in temporal or caudal space, etc. (see text for further detail). The curved line running from the rostral to the caudal SC is the horizontal meridian, which divides the representation of superior from the representation of inferior sensory space. Similarly, the curved line running from medial to lateral represents the vertical meridian, which divides ipsilateral and contralateral sensory space. Representative receptive fields (shading) for multisensory neurons from cat (left) and monkey (right) SC are drawn from rostral (top) and caudal (bottom) sites in the SC. Each concentric circle in the schematics of visual and auditory space represents 10°. In the representation of auditory space, the caudal half of contralateral space is shown by the split hemisphere that has been folded forward. Note the register among the receptive fields for visual-somatosensory and visual-auditory neurons. Visual receptive fields in nasal (frontal) space on the right are linked to somatosensory and auditory receptive fields in frontal space on the right. Similarly, temporal (or caudal) receptive fields in one modality are linked to similar locations in other modalities. Multisensory neurons are found in the deep layers of the SC. These layers are illustrated on a schematic of a coronal (vertical) section through the structure. S, superior; I, inferior; T, temporal; N, nasal; SZ, stratum zonale; SGS, stratum griseum superficiale; SO, stratum opticum; SGI, stratum griseum intermediale; SAI, stratum album intermediale; SGP, stratum griseum profundum; SAP, stratum album profundum.

and texture). However, the "sensory" topographies found in the SC do not serve this purpose and are thus quite distinct from those found in primary sensory structures. The principal function of the SC is to generate motor commands for the purpose of orienting to a sensory stimulus. Thus, whether one is dealing with a visual, auditory, or somatosensory stimulus, the problem is the same: to determine where the stimulus is with respect to the part of the body that must be oriented to it. For example, knowing where a visual stimulus is with respect to the fovea is not sufficient for programming a movement to reach out and grasp the object; for this, one needs to know where the stimulus is with respect to the hand. Similarly, knowing the location of an auditory stimulus with respect to the head is not sufficient to program an eye movement (i.e., gaze shift) to look at the stimulus; one needs to know where the stimulus is with respect to the current position of gaze. In other words, the topographic referent must be based on the structure or body part that is to be oriented toward the stimulus.

The SC is known to be involved in the generation of many types of orienting movements. The best established of these motor representations is the one that controls gaze. Therefore, the following description of the motor topography is based on what is known about gaze control, although in theory similar schemes could be constructed with ear or limb movement maps. Within the SC there is a gaze topography so that the site of activity codes for the distance and direction of a gaze shift. The components of this "motor" map are neurons that each have a "movement field," the motor analog of a sensory receptive field. Neurons with movement fields discharge in association with gaze shifts within a particular range of amplitude and direction and are arranged systematically according to this movement range; neurons that represent small contralateral movements are located in rostral SC; neurons representing progressively larger contralateral movements are located in progressively more caudal aspects of the structure. From medial to lateral in the SC the gradient is from neurons representing movements with upward directions to those representing movements with downward directions. The relationship between the SC sensory and motor representations is summarized as follows: The locus of sensory-evoked activity represents the location of a sensory stimulus with respect to the current gaze position; the location of motor-related activity represents the amplitude and direction of the movement required to shift gaze from the current position toward the location of the stimulus.

Tying the sensory topographies to the position of gaze ensures that the activity evoked by a sensory stimulus activates a region of the SC in which motor-related activity would be appropriate for shifting gaze to the stimulus. It also means that visual, auditory, and somatosensory stimuli share the same reference frame and will activate the same region of the SC if they originate from the same location in space. As such, the maps of visual, auditory, and somatosensory modalities will always be in register, regardless of the relative position of the eyes, head, and body to each other. The general alignment of these representations has been demonstrated in studies carried out in anesthetized animals with eyes, ears, head, and body facing forward so that the axes of visual, auditory, and tactile space are in approximate alignment with the direction of gaze. For each sensory modality, receptive fields shift systematically across space as one samples neurons in any given direction across the SC. For example, visual or auditory neurons in the rostral aspect of the SC have their receptive fields in central contralateral space (consistent with sites in the motor map that produce small contralateral gaze shifts), whereas those located progressively further rearward (caudal) in the structure have their receptive fields shifted progressively more eccentric into the peripheral aspects of contralateral space (in register with sites that produce larger contralateral gaze shifts). In short, when the animal is facing forward, neurons in the front of the structure represent the space in front of the animal and those in the rear of the structure represent space in the periphery. The somatosensory representation corresponds to this organization in that neurons with receptive fields on the face are located rostral in the SC and those with receptive fields progressively further back on the body (toward the rump) are located progressively more caudal. Neurons found medial in the structure have receptive fields in upper space (or on the upper body) and laterally located neurons have receptive fields progressively lower in space (or lower on the body).

Because many SC neurons are responsive to stimuli from more than one sensory modality, they contribute to the formation of multiple sensory representations in the SC. There are several varieties of SC multisensory neurons, and the order of incidence of bimodal neurons is as follows: visual-auditory, visual-soma-tosensory, and auditory-somatosensory. Although trimodal (visual-auditory-somatosensory) neurons are sometimes encountered, their incidence is comparatively low. However, regardless of its specific modality convergence pattern, each multisensory neuron has multiple receptive fields (Fig. 3), one for each of the sensory modalities to which it responds. As would be expected based on the topographic register described previously, the different receptive fields of each multisensory neuron correspond with each other (Fig. 3). One of the consequences of this receptive field correspondence is that any of the different sensory cues that are derived from the same event can activate the same neurons and thereby access the same circuitry to evoke a given orientation response. As discussed later, this cross-modal register of receptive fields is crucial for proper integration of the information derived from different sensory modalities.

2. Response Enhancement and Response Depression in Multisensory Neurons

Multisensory neurons do more than simply respond to a variety of different sensory stimuli: They transform the signals arriving from multiple sensory channels into an integrated multisensory product. In operational terms, multisensory integration is defined as a statistically significant difference between the number of impulses evoked by a cross-modal combination of stimuli (e.g., a visual and an auditory stimulus) and that evoked by the most effective of these stimuli alone. The integration results in either a response enhancement that can exceed the arithmetic sum of the individual modality-specific responses (Fig. 4), or a response depression that can eliminate responses altogether. The specific multisensory response that is achieved depends on the spatial relationships among the cross-modal stimuli. When two cross-modal stimuli are derived from the same event, they originate from the same location in space. Because the different receptive fields of the same multisensory neuron overlap one another in space, such an event can stimulate both excitatory receptive fields. These two inputs interact synergistically, and the degree to which the response is enhanced (above that evoked by the best modality-specific stimulus) depends on the relative effectiveness of these stimuli; combinations of weakly effective modality-specific stimuli usually result in the largest multisensory enhancements. Thus, multisensory enhancements are particularly beneficial when modality-specific stimuli are weak. If, on the other hand, the same cross-modal stimuli are spatially disparate, as would happen if they were derived from separate events, and one of them falls outside its receptive field, either no interaction results (the extrareceptive field stimulus produces no input to the neuron) or response depression is produced. The latter effect is generated when the extrareceptive field stimulus falls into an inhibitory region that borders the excitatory receptive field of some SC neurons, thereby generating an inhibitory input powerful enough to degrade or suppress the excitation produced by a stimulus within its receptive field.

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