bioRxiv Science⌕ Search

Biology subjects

Arbuckle, S. A.

Publications and source records attributed to Arbuckle, S. A..

4 recordsLinked to original sources

Mapping the integration of sensory information across fingers in human sensorimotor cortex

The integration of somatosensory signals across fingers is essential for dexterous object manipulation. Previous experiments suggest that this integration occurs in neural populations in the primary somatosensory cortex (S1). However, the integration process has not been fully characterized, as previous studies have mainly used two-finger stimulation paradigms. Here, we addressed this gap by stimulating all 31 single- and multi-finger combinations. We measured population-wide activity patterns evoked during finger stimulation in human S1 and primary motor cortex (M1) using 7T functional magnetic resonance imaging (fMRI) in female and male participants. Using multivariate fMRI analyses, we found clear evidence of unique non-linear interactions between fingers. In Brodmann area (BA) 3b, interactions predominantly occurred between pairs of neighbouring fingers. In BA 2, however, we found equally strong interactions between spatially distant fingers, as well as interactions between finger triplets and quadruplets. We additionally observed strong interactions in the hand area of M1. In both M1 and S1, these non-linear interactions did not reflect a general suppression of overall activity, suggesting instead that the interactions we observed reflect rich, non-linear integration of sensory inputs from the fingers. We suggest that this non-linear finger integration allows for a highly flexible mapping from finger sensory inputs to motor responses that facilitates dexterous object manipulation.

neuroscience↗

Structure of population activity in primary motor cortex for single finger flexion and extension

How is the primary motor cortex (M1) organized to control fine finger movements? We investigated the population activity in M1 for single finger flexion and extension, using 7T functional magnetic resonance imaging (fMRI) in female and male human participants, and compared these results to the neural spiking patterns recorded in two male monkeys performing the identical task. fMRI activity patterns were distinct for movements of different fingers, but quite similar for flexion and extension of the same finger. In contrast, spiking patterns in monkeys were quite distinct for both fingers and directions, similar to what was found for muscular activity patterns. The discrepancy between fMRI and electrophysiological measurements can be explained by two (non-mutually exclusive) characteristics of the organization of finger flexion and extension movements. Given that fMRI reflects predominantly input and recurrent activity, the results can be explained by an architecture in which neural populations that control flexion or extension of the same finger produce distinct outputs, but interact tightly with each other and receive similar inputs. Additionally, neurons tuned to different movement directions for the same finger (or combination of fingers) may cluster closely together, while neurons that control different finger combinations may be more spatially separated. When measuring this organization with fMRI at a coarse spatial scale, the activity patterns for flexion and extension of the same finger would appear very similar. Overall, we suggest that the discrepancy between fMRI and electrophysiological measurements provides new insights into the general organization of fine finger movements in M1. Significance statementThe primary motor cortex (M1) is important for producing individuated finger movements. Recent evidence shows that movements that commonly co-occur are associated with more similar activity patterns in M1. Flexion and extension of the same finger, which never co-occur, should therefore be associated with distinct representations. However, using carefully controlled experiments and multivariate analyses, we demonstrate that human fMRI activity patterns for flexion or extension of the same finger are highly similar. In contrast, spiking patterns measured in monkey M1 are clearly distinct. This suggests that populations controlling opposite movements of the same finger, while producing distinct outputs, may cluster together and share inputs and local processing. These results provide testable hypotheses about the organization of hand control in M1.

neuroscience↗

Stability of representational geometry across a wide range of fMRI activity levels

Fine-grained activity patterns, as measured with functional magnetic resonance imaging (fMRI), are thought to reflect underlying neural representations. Multivariate analysis techniques, such as representational similarity analysis (RSA), can be used to test models of brain representation by quantifying the representational geometry (the collection of pair-wise dissimilarities between activity patterns). One important caveat, however, is that non-linearities in the coupling between neural activity and the fMRI signal may lead to significant distortions in the representational geometry estimated from fMRI activity patterns. Here we tested the stability of representational dissimilarity measures in primary sensory-motor (S1 and M1) and early visual regions (V1/V2) across a large range of activation levels. Subjects were visually cued with different letters to perform single finger presses with one of the 5 fingers at a rate of 0.3-2.6 Hz. For each stimulation frequency, we quantified the difference between the 5 activity patterns in M1, S1, and V1/V2. We found that the representational geometry remained stable, even though the average activity increased over a large dynamic range. These results indicate that the representational geometry of fMRI activity patterns can be reliably assessed, largely independent of the average activity in the region. This has important methodological implications for RSA and other multivariate analysis approaches that use the representational geometry to make inferences about brain representations.

neuroscience↗

Does human primary motor cortex represent sequences of finger movements?

Human primary motor cortex (M1) is an essential structure for the production of dexterous hand movements. While distinct sub-populations of neurons are activated during single finger movements, it remains unknown whether M1 also represents sequences of multiple finger movements. Using novel multivariate fMRI analysis techniques, we show here that even after 5 days of intense practice there was little or no evidence for a true sequence representation in M1. Rather, the activity patterns for sequences in M1 could be explained by linear combination of patterns associated with the constituent individual finger movements, with the strongest weight on the finger making the first response of the sequence. These results suggest that M1 only represents single finger movements, but receives increased input at the start of a sequence. In contrast, the reliable differences between different sequences in premotor and parietal areas could not be explained by a strong weighting of the first finger, supporting the view that these regions exhibit a true representation of sequences.

neuroscience↗