Abstract The cerebellum regulates nonmotor behavior, but the routes of influence are not well characterized. Here we report a necessary role for the posterior cerebellum in guiding a reversal learning task through a network of diencephalic and neocortical structures, and in flexibility of free behavior. After chemogenetic inhibition of lobule VI vermis or hemispheric crus I Purkinje cells, mice could learn a water Y-maze but were impaired in ability to reverse their initial choice. To map targets of perturbation, we imaged c-Fos activation in cleared whole brains using light-sheet microscopy. Reversal learning activated diencephalic and associative neocortical regions. Distinctive subsets of structures were altered by perturbation of lobule VI (including thalamus and habenula) and crus I (including hypothalamus and prelimbic/orbital cortex), and both perturbations influenced anterior cingulate and infralimbic cortex. To identify functional networks, we used correlated variation in c-Fos activation within each group. Lobule VI inactivation weakened within-thalamus correlations, while crus I inactivation divided neocortical activity into sensorimotor and associative subnetworks. In both groups, high-throughput automated analysis of whole-body movement revealed deficiencies in across-day behavioral habituation to an open-field environment. Taken together, these experiments reveal brainwide systems for cerebellar influence that affect multiple flexible responses.
more »
« less
The Cerebellum Is Sensitive to the Lexical Properties of Words During Spoken Language Comprehension
Over the past few decades, research into the function of the cerebellum has expanded far beyond the motor domain. A growing number of studies are probing the role of specific cerebellar subregions, such as Crus I and Crus II, in higher-order cognitive functions including receptive language processing. In the current fMRI study, we show evidence for the cerebellum’s sensitivity to variation in two well-studied psycholinguistic properties of words—lexical frequency and phonological neighborhood density—during passive, continuous listening of a podcast. To determine whether, and how, activity in the cerebellum correlates with these lexical properties, we modeled each word separately using an amplitude-modulated regressor, time-locked to the onset of each word. At the group level, significant effects of both lexical properties landed in expected cerebellar subregions: Crus I and Crus II. The BOLD signal correlated with variation in each lexical property, consistent with both language-specific and domain-general mechanisms. Activation patterns at the individual level also showed that effects of phonological neighborhood and lexical frequency landed in Crus I and Crus II as the most probable sites, though there was activation seen in other lobules (especially for frequency). Although the exact cerebellar mechanisms used during speech and language processing are not yet evident, these findings highlight the cerebellum’s role in word-level processing during continuous listening.
more » « less- NSF-PAR ID:
- 10473419
- Publisher / Repository:
- DOI PREFIX: 10.1162
- Date Published:
- Journal Name:
- Neurobiology of Language
- ISSN:
- 2641-4368
- Format(s):
- Medium: X Size: p. 1-17
- Size(s):
- ["p. 1-17"]
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
more » « less
This exploratory study examined the simultaneous interactions and relative contributions of bottom-up social information (regional dialect, speaking style), top-down contextual information (semantic predictability), and the internal dynamics of the lexicon (neighborhood density, lexical frequency) to lexical access and word recognition. Cross-modal matching and intelligibility in noise tasks were conducted with a community sample of adults at a local science museum. Each task featured one condition in which keywords were presented in isolation and one condition in which they were presented within a multiword phrase. Lexical processing was slower and more accurate when keywords were presented in their phrasal context, and was both faster and more accurate for auditory stimuli produced in the local Midland dialect. In both tasks, interactions were observed among stimulus dialect, speaking style, semantic predictability, phonological neighborhood density, and lexical frequency. These interactions revealed that bottom-up social information and top-down contextual information contribute more to speech processing than the internal dynamics of the lexicon. Moreover, the relatively stronger bottom-up social effects were observed in both the isolated word and multiword phrase conditions, suggesting that social variation is central to speech processing, even in non-interactive laboratory tasks. At the same time, the specific interactions observed differed between the two experiments, reflecting task-specific demands related to processing time constraints and signal degradation.
-
more » « less
In most environments, the visual system is confronted with many relevant objects simultaneously. That is especially true during reading. However, behavioral data demonstrate that a serial bottleneck prevents recognition of more than one word at a time. We used fMRI to investigate how parallel spatial channels of visual processing converge into a serial bottleneck for word recognition. Participants viewed pairs of words presented simultaneously. We found that retinotopic cortex processed the two words in parallel spatial channels, one in each contralateral hemisphere. Responses were higher for attended than for ignored words but were not reduced when attention was divided. We then analyzed two word-selective regions along the occipitotemporal sulcus (OTS) of both hemispheres (subregions of the visual word form area, VWFA). Unlike retinotopic regions, each word-selective region responded to words on both sides of fixation. Nonetheless, a single region in the left hemisphere (posterior OTS) contained spatial channels for both hemifields that were independently modulated by selective attention. Thus, the left posterior VWFA supports parallel processing of multiple words. In contrast, activity in a more anterior word-selective region in the left hemisphere (mid OTS) was consistent with a single channel, showing (
i ) limited spatial selectivity, (ii ) no effect of spatial attention on mean response amplitudes, and (iii ) sensitivity to lexical properties of only one attended word. Therefore, the visual system can process two words in parallel up to a late stage in the ventral stream. The transition to a single channel is consistent with the observed bottleneck in behavior. -
Human speech perception involves transforming a countinuous acoustic signal into discrete linguistically meaningful units (phonemes) while simultaneously causing a listener to activate words that are similar to the spoken utterance and to each other. The Neighborhood Activation Model posits that phonological neighbors (two forms [words] that differ by one phoneme) compete significantly for recognition as a spoken word is heard. This definition of phonological similarity can be extended to an entire corpus of forms to produce a phonological neighbor network (PNN). We study PNNs for five languages: English, Spanish, French, Dutch, and German. Consistent with previous work, we find that the PNNs share a consistent set of topological features. Using an approach that generates random lexicons with increasing levels of phonological realism, we show that even random forms with minimal relationship to any real language, combined with only the empirical distribution of language-specific phonological form lengths, are sufficient to produce the topological properties observed in the real language PNNs. The resulting pseudo-PNNs are insensitive to the level of lingustic realism in the random lexicons but quite sensitive to the shape of the form length distribution. We therefore conclude that “universal” features seen across multiple languages are really string universals, not language universals, and arise primarily due to limitations in the kinds of networks generated by the one-step neighbor definition. Taken together, our results indicate that caution is warranted when linking the dynamics of human spoken word recognition to the topological properties of PNNs, and that the investigation of alternative similarity metrics for phonological forms should be a priority.more » « less
-
more » « less
Objective Increasing evidence suggests that cerebellar damage impacts on cognitive functions. Frontotemporal dementias (FTDs) are neurodegenerative brain conditions, primarily affecting the frontal and/or temporal lobe. Three main phenotypes are recognized, each with a distinct clinical and cognitive profile: behavioral‐variant FTD (bvFTD), semantic dementia (SD), and progressive nonfluent aphasia (PNFA). The severity of cerebellar changes and their relation to cognition in FTD, however, remain unclear. This study aimed to establish cerebellar gray matter changes on magnetic resonance imaging (MRI) and their relation to profiles of cognitive deficits in FTD subtypes.
Methods Ninety‐six FTD patients (45 bvFTD, 28 SD, and 23 PNFA), meeting current clinical diagnostic criteria, and 35 age‐, sex‐, and education‐matched controls underwent brain MRI and cognitive assessment. Cerebral and cerebellar gray matter integrity were investigated using voxel‐based morphometry.
Results Compared with controls, widespread bilateral cerebellar changes were observed in all FTD subtypes, with the greatest atrophy present in bvFTD. Significant associations were found between cerebellar integrity and cognitive performance in attention and working memory in bvFTD, visuospatial function in SD, and language‐motor function in PNFA. Bilateral atrophy of crus and lobule VI were most commonly associated with cognitive deficits, irrespective of FTD phenotype.
Interpretation This study is the first to identify distinct patterns of cerebellar atrophy across FTD syndromes, which in turn relate to discrete cognitive dysfunctions, after accounting for the effect of cerebral atrophy. These findings extend our understanding of the cerebellum and point to its involvement across an array of processes beyond the domain of motor function. Ann Neurol 2018;83:98–109
