Possible anatomical pathways for short-latency multisensory integration processes in primary sensory cortices

Abstract

Multisensory integration does not only recruit higher-level association cortex, but also low-level and even primary sensory cortices. Here, we will describe and quantify two types of anatomical pathways, a thalamocortical and a corticocortical that possibly underlie short-latency multisensory integration processes in the primary auditory (A1), somatosensory (S1), and visual cortex (V1). Results were obtained from Mongolian gerbils, a common model-species in neuroscience, using simultaneous injections of different retrograde tracers into A1, S1, and V1. Several auditory, visual, and somatosensory thalamic nuclei project not only to the primary sensory area of their own (matched) but also to areas of other (non-matched) modalities. The crossmodal output ratios of these nuclei, belonging to both core and non-core sensory pathways, vary between 0.4 and 63.5 % of the labeled neurons. Approximately 0.3 % of the sensory thalamic input to A1, 5.0 % to S1, and 2.1 % to V1 arise from non-matched nuclei. V1 has most crossmodal corticocortical connections, projecting strongest to S1 and receiving a similar amount of moderate inputs from A1 and S1. S1 is mainly interconnected with V1. A1 has slightly more projections to V1 than S1, but gets just faint inputs from there. Concerning the layer-specific distribution of the retrogradely labeled somata in cortex, V1 provides the most pronounced feedforward-type outputs and receives (together with S1) most pronounced feedback-type inputs. In contrast, A1 has most pronounced feedback-type outputs and feedforward-type inputs in this network. Functionally, the different sets of thalamocortical and corticocortical connections could underlie distinctive types of integration mechanisms for different modality pairings.

Long, intrinsic horizontal axons radiating through and beyond rat barrel cortex have spatial distributions similar to horizontal spreads of activity evoked by whisker stimulation

“…In rat barrel cortex, horizontal projections have generally been described as extending only one or two barrel diameters in any given direction for pyramidal neurons in barrel columns, and for two to four barrel diameters in any given direction for neurons in septal columns, although evidence for a sparser projection beyond this extent often has been present in photomicrographs (Chapin et al 1987; Koralek et al 1990, Bernardo et al 1990; Fabri and Burton 1991; Hoeflinger et al 1995; Gottlieb and Keller 1997; Kim and Ebner 1999; Broser et al 2008; Oberlaender et al 2011; Lee et al 2011; Kim and Lee 2013; Narayanan et al 2015). Prior studies in rats (Miller and Vogt 1984; Paperna and Malach 1991) and other rodents (Budinger et al 2006; Larsen et al 2009; Campi et al 2007; 2010; Charbonneau et al 2012; Laramée et al 2013; Henschke et al 2015) resulted in reports of sparse projections from somatosensory cortex to other primary sensory cortices, but most of these studies employed retrograde neuronal tracers and therefore could not have appreciated that the axons involved coursed diffusely through gray matter, branching along the way. Although neurons in the barrel field are known to have long projections to the dysgranular zone of the somatosensory cortex and to the posterior parietal cortex (Kim and Ebner 1999; Oberlaender et al 2011; Lee et al 2011; Kim and Lee 2013), these axons typically are not discussed as being abundant in other associational cortices posterior to PMBSF.…”

Where are multisensory signals combined for perceptual decision-making?

“…[17][18][19][20]] and anatomical [ [21], e.g. [22][23][24][25]] evidence for multisensory interactions in primary and non-primary sensory cortices.…”

Species-dependent role of crossmodal connectivity among the primary sensory cortices

“…In cats, non-auditory inputs represent approximately 11.3% of the total ipsilateral corticocortical projection to A1 (Chabot et al, 2015), 13% to AAF (Wong et al, 2015), and 7% to PAF (Butler et al, 2016a) which are all tonotopically organized, while non-auditory afferents to higher-level auditory areas represent approximately 52% of the inputs to area DZ (Kok et al, 2013) and 59% to the FAES (Meredith et al, 2016). Connectional studies of A1 in other species also report non-auditory cortical sources of inputs, including rats (Paperna and Malach, 1991), voles (Campi et al, 2010) and gerbils (Henschke et al, 2015). Ultimately, these connectional data are consistent with the modality distribution of neuronal responsiveness observed by electrophysiological recording, as illustrated in Figure 1.…”