Measuring the effects of attention to individual fingertips in somatosensory cortex using ultra-high field (7T) fMRI

Highlights

• Attending to tactile stimulation modulates primary somatosensory cortex, S1.

• High-resolution fMRI at 7T can measure fingertip specific attentional modulation.

• This modulation is somatotopically appropriate and directly linked to task-relevance.

• Such measurements are critical for examining neural mechanisms of somatosensation.

Abstract

Attention to sensory information has been shown to modulate the neuronal processing of that information. For example, visuospatial attention acts by modulating responses at retinotopically appropriate regions of visual cortex (Puckett and DeYoe, 2015, Tootell et al., 1998). Much less, however, is known about the neuronal processing associated with attending to other modalities of sensory information. One reason for this is that visual cortex is relatively large, and therefore easier to access non-invasively in humans using tools such as functional magnetic resonance imaging (fMRI). With high-resolution fMRI, however, it is now possible to access smaller cortical areas such as primary somatosensory cortex (Martuzzi et al., 2014; Sanchez-Panchuelo et al., 2010; Schweisfurth et al. 2014; Schweizer et al. 2008). Here, we combined a novel experimental design and high-resolution fMRI at ultra-high field (7T) to measure the effects of attention to tactile stimulation in primary somatosensory cortex, S1. We find that attention modulates somatotopically appropriate regions of S1, and importantly, that this modulation can be measured at the level of the cortical representation of individual fingertips.

Introduction

Attention to incoming sensory information has been shown to modulate neuronal responses and subsequently alter perception of that information and, accordingly, influence behavior (Driver, 2001). To date, the majority of attention research has investigated the processing of visual and auditory information, with a lesser focus on other sensory modalities such as somatosensation. It is clear, however, that people are able to voluntarily direct their attention to a part of their body and that doing so speeds up processing of somatosensory information at that location (Spence and Gallace, 2007). Understanding how attentional processes interact with the cortical processing of sensory information is, thus, central to understanding the neural basis of human somatosensation.

The neuronal processing of tactile information occurs in humans, in large part, in primary somatosensory cortex, S1 (Kandel et al., 2000). Early demonstrations of tactile stimulation eliciting focal neuronal activation within human S1 were performed using Positron Emission Tomography (PET) (Fox et al., 1987, Greenberg et al., 1981). Using fMRI, it became possible to further resolve this activation to individuate the responses to stimulation of individual fingers (Francis et al., 2000, Gelnar et al., 1998; Schweisfurth et al., 2014, Schweizer et al., 2008). More recently, research employing high-resolution fMRI has revealed that human S1 contains multiple orderly somatotopic maps of the fingers, both across digits (Maldjian et al., 1999, Martuzzi et al., 2014, Sanchez-Panchuelo et al., 2010) and within digits (Sanchez-Panchuelo et al., 2012).

Human neuroimaging studies have also investigated the influence of attention in somatosensory cortex finding that attention modulates activity in a number of cortical areas, including early somatosensory cortex (Burton and Sinclair, 2000). For example, using PET it has been shown that attention to tactile information modulates activity in S1 (Meyer et al., 1991, Roland, 1981). Supporting these findings, studies using fMRI have shown that Blood Oxygenation Level Dependent (BOLD) signals elicited in S1 are greater for attended compared to actively ignored (Sterr et al., 2007) or passively experienced (Nelson et al., 2004) tactile stimulation. Although this work has provided clear evidence that attentional modulation occurs at regions of somatotopically organized cortex, these measurements have been rather limited, considering only a single finger, or toe (Johansen-Berg et al., 2000). The limited nature of the measurements in the studies reporting attentional modulation in S1 along with the fact that there have been other studies that have failed to demonstrate robust modulation in S1 during active attention to somatosensory information (Backes et al., 2000, Mima et al., 1998) highlight the need for additional investigation.

Here we show that attending to tactile stimulation does indeed modulate somatotopically appropriate regions in S1 and that using high-resolution fMRI allows these effects to be measured at the spatial scale necessary to resolve modulation associated with attending to each individual fingertip. The fact that attention is able to differentially modulate neuronal responses when attending to individual fingertips is in line with known, touch-related behavioral abilities of humans that require individuation of sensory information at each fingertip such as haptic exploration and tactile object recognition (Lederman and Klatzky, 2009). Moreover, the ability to measure this attention-related modulation in awake and behaving humans promises a better understanding of the neural basis of attentional processes and how they influence our perception of somatosensory information.