Temporal profiles of response enhancement in multisensory integration

Abstract

Animals have evolved multiple senses that transduce different forms of energy as a way of increasing their sensitivity to environmental events. Each sense provides a unique and independent perspective on the world, and very often a single event stimulates several of them. In order to make best use of the available information, the brain has also evolved the capacity to integrate information across the senses ("multisensory integration"). This facilitates the detection, localization, and identification of a given event, and has obvious survival value for the individual and the species. Multisensory responses in the superior colliculus (SC) evidence shorter latencies and are more robust at their onset. This is the phenomenon of initial response enhancement in multisensory integration, which is believed to represent a real time fusion of information across the senses. The present paper reviews two recent reports describing how the timing and robustness of sensory responses change as a consequence of multisensory integration in the model system of the SC.

Keywords: cross-modal; enhancement; latency; multisensory; superior colliculus.

Figure 1

A schematic model of the circuit believed to support multisensory integration in the superior colliculus (SC). A multisensory (visual-auditory) neuron receives input from a number of unisensory sources; in particular, inputs derived from areas of association cortex (e.g., AES) (top) and inputs from other sources (bottom). These inputs also project to an inhibitory interneuron population (I). The inhibitory connections “offset,” or balance, the excitatory inputs, but have a greater impact on non-AES than AES inputs. The balance of excitation and inhibition in this single-unit model replicates a number of physiological findings pertaining to multisensory integration in the SC; for example, its dependence on the functional integrity of cortico-collicular afferents from AES. The nature of the biophysical mechanisms underlying multisensory integration remains an active area of empirical enquiry.

Figure 2

Two different models for the temporal profile of multisensory integration. Illustrated are putative unisensory visual (V), auditory (A), and multisensory (VA) input magnitudes (top) and cumulative output magnitudes (bottom) as a function of time. If inputs are integrated in real-time (left, A), the multisensory input magnitude will cross threshold earlier than either unisensory input (upper-left). This will produce a multisensory response with a shorter response latency and higher initial firing rate. The predicted cumulative response profile (qsum) is illustrated in the lower-left corner. Alternatively, if multisensory integration takes place only later in the response (“delayed integration”, B), the multisensory and unisensory input profiles will initially appear similar, but the multisensory response will reach a higher peak (upper-right). This will yield multisensory responses that are enhanced in magnitude, but have identical physiological response latencies as the unisensory responses (bottom-right).

Figure 3

Multisensory integration reflects an initial response enhancement (IRE). Shown is a dramatic example of initial response enhancement from a single visual-auditory SC neuron. Impulse rasters for visual (V), auditory (A), and multisensory (VA) responses are displayed on the left. The vertical line crossing each plot indicates the time of the multisensory response onset, with respect to which the unisensory responses are delayed. The differences between the multisensory and unisensory qsums (upper-right) and event estimates (lower-right) are striking. The multisensory response not only evidences a shorter latency, but is greatly enhanced in robustness from its very onset.