The timing and laminar profile of converging inputs to multisensory areas of the macaque neocortex

Abstract

Two fundamental requirements for multisensory integration are convergence of unisensory (e.g. visual and auditory) inputs and temporal alignment of the neural responses to convergent inputs. We investigated the anatomic mechanisms of multisensory convergence by examining three areas in which convergence occurs, posterior auditory association cortex, superior temporal polysensory area (STP) and ventral intraparietal sulcus area (VIP). The first of these was recently shown to be a site of multisensory convergence and the latter two are more well known as ‘classic’ multisensory regions. In each case, we focused on defining the laminar profile of response to the unisensory inputs. This information is useful because two major types of connection, feedforward and feedback, have characteristic differences in laminar termination patterns, which manifest physiologically. In the same multisensory convergence areas we also examined the timing of the unisensory inputs using the same standardized stimuli across all recordings. Our findings indicate that: (1) like somatosensory input [J. Neurophysiol., 85 (2001) 1322], visual input is available at very early stages of auditory processing, (2) convergence occurs through feedback, as well as feedforward anatomical projections and (3) input timing may be an asset, as well as a constraint in multisensory processing.

Introduction

Multisensory integration is essential for the production of the seamless, unified representation of the world that we experience subjectively. This integration requires the anatomical convergence of unisensory inputs onto single neurons or ensembles of interconnected neurons [46], and some degree of temporal alignment of the unisensory inputs [54]. A detailed explication of the brain mechanisms of multisensory processing has been conducted in the carnivore superior colliculus (reviewed by Stein and Meredith [54]), and substantial progress has also been made at the neocortical level, most notably in monkeys [1], [2], [8], [15], [16], [19], [20], [24], [25], [27], [36], [37], [38], [52] and more recently in humans [4], [5], [7], [10], [12], [21], [30].

Despite these advances, large questions remain about the anatomical substrates of multisensory convergence in primates. We know, for example, that several ‘classic’ multisensory regions, including the superior temporal polysensory area, or STP [53], and the intraparietal (IP) sulcus [52] do receive converging ascending (feedforward) sensory inputs. However, several cortical areas at low levels in their respective sensory processing hierarchies have been shown or suggested to be sites of multisensory convergence, including auditory association cortex [7], [45] and the human MT+ complex [4], [5], and these areas have not been shown to receive the appropriate feedforward convergence of sensory inputs. In fact, the lack of the clear anatomical substrate for multisensory convergence has led to the speculation that convergence in these ‘unisensory’ areas occurs through combination of feedforward and feedback inputs [6]. Similarly large questions remain about the temporal parameters of the converging sensory inputs. We know that there is a temporal window for integration of neural responses to stimulus inputs from different modalities, as well as for our perception of multisensory inputs as ‘fused’ (i.e. relating to the same object (reviewed by Stein and Meredith [55])). However, the timing of sensory inputs to neocortex has received very little attention, beyond a few studies of response latencies in the visual system [14], [32], [44], [47]. Virtually nothing is known about the timing of convergent multisensory inputs in different cortical structures, and the picture becomes much more complex when the combination of feedforward and feedback input is invoked.

In the present study, we investigated the laminar profile and the timing of sensory inputs in several of the primate neocortical areas in which multisensory convergence occurs. The laminar profile of sensory activation is of interest because it can help to distinguish between feedforward and feedback inputs, due to their differing laminar termination patterns [45], [47]. We investigated posterior auditory association cortex, which our recent studies show to be a multisensory region [45], and compared the timing and laminar profile of auditory, somatosensory and visual responses in this region to those of corresponding responses in more ‘classic’ multisensory regions including the superior temporal polysensory (STP) area, and lateral and ventral intraparietal (IP) Areas. Our findings indicate that: (1) like somatosensory input [45], visual input is available at very early stages of auditory processing, (2) convergence occurs through feedback, as well as feedforward anatomical projections and (3) input timing may be an asset, as well as a constraint in multisensory processing.