Highlights d Privileged human auditory to ventral prefrontal connectivity, paralleled in monkeys d Common auditory to parahippocampal effective connectivity in both species d Stronger lateralization of connectivity effects in humans than in monkeys d Human fronto-temporal network rooted in conserved organizational principle
Highlights 22 • Privileged human auditory to inferior frontal connectivity, linked to monkeys 23 • Common auditory to parahippocampal effective connectivity in both species 24 • Greater lateralization in human effective connectivity, more symmetrical in monkeys 25 • Human fronto-temporal network function rooted in evolutionarily conserved signature 26 27 eTOC short summary 28 Functional connectivity between regions crucial for language and declarative memory is thought to 29 have substantially differentiated in humans. Using a new technique to similarly visualize directional 30 effective connectivity in humans and monkeys, we found remarkably comparable connectivity patterns 31 in both species between fronto-temporal regions crucial for cognition. 32 33 ABSTRACT 36 Cognitive pathways supporting human language and declarative memory are thought to have uniquely 37 evolutionarily differentiated in our species. However, cross-species comparisons are missing on site-38 specific effective connectivity between regions important for cognition. We harnessed a new approach 39 using functional imaging to visualize the impact of direct electrical brain stimulation in human 40 neurosurgery patients. Applying the same approach with macaque monkeys, we found remarkably 41 comparable patterns of effective connectivity between auditory cortex and ventro-lateral prefrontal 42 cortex (vlPFC) and parahippocampal cortex in both species. Moreover, in humans electrical 43 tractography revealed rapid evoked potentials in vlPFC from stimulating auditory cortex and speech 44 sounds drove vlPFC, consistent with prior evidence in monkeys of direct projections from auditory 45 cortex to vocalization responsive regions in vlPFC. The results identify a common effective 46 connectivity signature that from auditory cortex is equally direct to vlPFC and indirect to the homology, convergence or divergence, can be of substantial theoretical significance: Within the motor 52 domain, human and nonhuman primates have direct cortico-spinal projections subserving fine 53 movement control that are indirect in rodents 1 . Also, human laryngeal motor cortex projects directly to 54 a brain stem nucleus (ambiguus) controlling laryngeal muscles 2 . Such projections for vocal production 55 are more indirect in nonhuman primates 3 and rodents 4 , shedding light on human speech evolution 5 . 56 Language defines us as a species and because of its prominent role in declarative memory 57 substantial evolutionary differentiation of human cognitive pathways is expected. Comparative studies 58 often see considerable levels of evolutionary conservation alongside insights on species-specific 59 differences 6-12 . Yet, certain cross-species comparisons are missing, such as on the impact of directed 60 effective connectivity with the required precision of site-specific perturbation that can be applied to 61 both human and nonhuman primates. Thereby, the question on the extent of differentiation versus 62 conservation in primate fronto-temporal systems-although crucial fo...
Visual attention is captured by transient signals in the periphery of the visual field, allowing enhanced perceptual representations in spatial tasks. However, it has been reported that the same cues impair performance in temporal tasks (e.g., Yeshurun, 2004; Yeshurun & Levy, 2003). This findings suggest that transient attention enhances the activity of slow, high-resolution channels, like parvocellular neurons, and/or shuts off faster channels better sensitive to low spatial frequencies, such as the ones of the magnocellular system. To test this idea, we have measured the spatio-temporal perceptive fields for transiently cued signals at various eccentricities using the classification images (CI) technique. At near eccentricities transient attention caused the perceptual templates to be sharper in space and characterized by much stronger high spatial frequency components. At the same time, they show a consistently larger temporal integration window. These effects of attention on perceptual filters are strongly reduced at far eccentricities and disappear when using longer target-cue lags. These data provide evidence in support of the parvocellular model of transient, exogenous attention, showing that in the presence of a well timed spatial cue observers rely on noisy evidence lasting longer and with finer spatial configurations.
The detectability of target sounds embedded within noisy backgrounds is affected by the regularities that summarize acoustic sceneries. Previous studies suggested that the dynamic range of neurons in the inferior colliculus (IC) of anesthetized guinea pigs shifts toward the mean sound pressure level in irregular acoustic environments. Yet, it is unclear how this neuronal adaptation processes may influence the effectiveness of sounds as a masker, both behaviorally and in terms of neuronal encoding. To answer this question, we measured the neural response of IC neurons while macaque monkeys performed a Go/No-Go tone detection task. Macaques detected a 50-ms tone that was either simultaneously gated with a burst of noise or embedded within a continuous noise background, whose levels were randomly sampled (every 50 ms) from a probability distribution. The mean of the distribution matched the level of the gated burst of noise. Psychometric and IC neurometric thresholds to tones did not differ between the two masking conditions. However, the neuronal firing rate versus level function was significantly affected by the temporal characteristics of the noise masker. Simultaneously gated noise caused higher baseline responses and greater dynamic range compression compared with noise distribution. The slopes of psychometric and neurometric functions were significantly shallower for higher variance distributions, suggesting that neuronal sensitivity might change with the variability of the sound. Our results suggest that the adaptive response of IC neurons to sound regularities does not affect the effectiveness of the noise-masking signal, which remains invariant to surrounding noise amplitudes. NEW & NOTEWORTHY Auditory neurons adapt to the statistics of sound levels in the acoustic scene. However, it is still unclear to what extent such adaptation influences the effectiveness of the stimulus as a masker. Our study represents the first attempt to investigate how the adaptation to the statistics of masking stimuli may be related to the effectiveness of masking, and to the single-unit encoding of the midbrain auditory neurons in behaving animals.
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