Spatial frequency tuning of motor responses reveals differential contribution of dorsal and ventral systems to action comprehension

Understanding object-directed actions performed by others is central to everyday life. This ability is thought to rely on the interaction between the dorsal action observation network (AON) and a ventral object recognition pathway. On this view, the AON would encode action kinematics, and the ventral pathway, the most likely intention afforded by the objects. However, experimental evidence supporting this model is still scarce. Here, we aimed to disentangle the contribution of dorsal vs. ventral pathways to action comprehension by exploiting their differential tuning to low-spatial frequencies (LSFs) and high-spatial frequencies (HSFs). We filtered naturalistic action images to contain only LSF or HSF and measured behavioral performance and corticospinal excitability (CSE) using transcranial magnetic stimulation (TMS). Actions were embedded in congruent or incongruent scenarios as defined by the compatibility between grips and intentions afforded by the contextual objects. Behaviorally, participants were better at discriminating congruent actions in intact than LSF images. This effect was reversed for incongruent actions, with better performance for LSF than intact and HSF. These modulations were mirrored at the neurophysiological level, with greater CSE facilitation for congruent than incongruent actions for HSF and the opposite pattern for LSF images. Finally, only for LSF did we observe CSE modulations according to grip kinematics. While results point to differential dorsal (LSF) and ventral (HSF) contributions to action comprehension for grip and context encoding, respectively, the negative congruency effect for LSF images suggests that object processing may influence action perception not only through ventral-to-dorsal connections, but also through a dorsal-to-dorsal route involved in predictive processing.

Developmental variability channels mouse molar evolution

Do developmental systems preferentially produce certain types of variation that orient phenotypic evolution along preferred directions? At different scales, from the intra-population to the interspecific, the murine first upper molar shows repeated anterior elongation. Using a novel quantitative approach to compare the development of two mouse strains with short or long molars, we identified temporal, spatial and functional differences in tooth signaling center activity, that arise from differential tuning of the activation-inhibition mechanisms underlying tooth patterning. By tracing their fate, we could explain why only the upper first molar reacts via elongation of its anterior part. Despite a lack of genetic variation, individuals of the elongated strain varied in tooth length and the temporal dynamics of their signaling centers, highlighting the intrinsic instability of the upper molar developmental system. Collectively, these results reveal the variational properties of murine molar development that drive morphological evolution along a line of least resistance.

The making of an olfactory specialist

The evolution of animal behaviour is poorly understood. Despite numerous correlations of behavioural and nervous system divergence, demonstration of the genetic basis of interspecific behavioural differences remains rare. Here we develop a novel neurogenetic model, Drosophila sechellia, a close cousin of D. melanogaster that displays profound behavioural changes linked to its extreme host fruit specialisation. Through calcium imaging, we identify olfactory pathways detecting host volatiles. Mutational analysis indicates roles for individual receptors in long- and short-range attraction. Cross-species allele transfer demonstrates that differential tuning of one receptor is important for species-specific behaviour. We identify the molecular determinants of this functional change, and characterise their behavioural significance and evolutionary origin. Circuit tracing reveals that receptor adaptations are accompanied by increased sensory pooling onto interneurons and novel central projection patterns. This work links molecular and neuronal changes to behavioural divergence and defines a powerful model for investigating nervous system evolution and speciation.

Differential Tuning of Ventral and Dorsal Streams during the Generation of Common and Uncommon Tool Uses

Our use of tools is situated in different contexts. Prior evidence suggests that diverse regions within the ventral and dorsal streams represent information supporting common tool use. However, given the flexibility of object concepts, these regions may be tuned to different types of information when generating novel or uncommon uses of tools. To investigate this, we collected fMRI data from participants who reported common or uncommon tool uses in response to visually presented familiar objects. We performed a pattern dissimilarity analysis in which we correlated cortical patterns with behavioral measures of visual, action, and category information. The results showed that evoked cortical patterns within the dorsal tool use network reflected action and visual information to a greater extent in the uncommon use group, whereas evoked neural patterns within the ventral tool use network reflected categorical information more strongly in the common use group. These results reveal the flexibility of cortical representations of tool use and the situated nature of cortical representations more generally.

Hsf1 phosphorylation generates cell-to-cell variation in Hsp90 levels and promotes phenotypic plasticity

ABSTRACTClonal populations of cells exhibit cell-to-cell variation in the transcription of individual genes. In addition to this “noise” in gene expression, heterogeneity in the proteome and the proteostasis network expands the phenotypic diversity of a population. Heat shock transcription factor (Hsf1) regulates chaperone gene expression, thereby coupling transcriptional noise to proteostasis. Here we show that cell-to-cell variation in Hsf1 activity is an important determinant of phenotypic plasticity. Budding yeast cells with high Hsf1 activity were enriched for the ability to acquire resistance to an antifungal drug, and this enrichment depended on Hsp90 – a known “phenotypic capacitor” and canonical Hsf1 target. We show that Hsf1 phosphorylation promotes cell-to-cell variation, and this variation – rather than absolute Hsf1 activity – promotes antifungal resistance. We propose that Hsf1 phosphorylation enables differential tuning of the proteostasis network in individual cells, allowing populations to access a wide range of phenotypic states.

Temporal Tuning of Word- and Face-selective Cortex

Sensitivity to temporal change places fundamental limits on object processing in the visual system. An emerging consensus from the behavioral and neuroimaging literature suggests that temporal resolution differs substantially for stimuli of different complexity and for brain areas at different levels of the cortical hierarchy. Here, we used steady-state visually evoked potentials to directly measure three fundamental parameters that characterize the underlying neural response to text and face images: temporal resolution, peak temporal frequency, and response latency. We presented full-screen images of text or a human face, alternated with a scrambled image, at temporal frequencies between 1 and 12 Hz. These images elicited a robust response at the first harmonic that showed differential tuning, scalp topography, and delay for the text and face images. Face-selective responses were maximal at 4 Hz, but text-selective responses, by contrast, were maximal at 1 Hz. The topography of the text image response was strongly left-lateralized at higher stimulation rates, whereas the response to the face image was slightly right-lateralized but nearly bilateral at all frequencies. Both text and face images elicited steady-state activity at more than one apparent latency; we observed early (141–160 msec) and late (>250 msec) text- and face-selective responses. These differences in temporal tuning profiles are likely to reflect differences in the nature of the computations performed by word- and face-selective cortex. Despite the close proximity of word- and face-selective regions on the cortical surface, our measurements demonstrate substantial differences in the temporal dynamics of word- versus face-selective responses.