Language networks in anophthalmia: maintained hierarchy of processing in ‘visual’ cortex

Abstract

Imaging studies in blind subjects have consistently shown that sensory and cognitive tasks evoke activity in the occipital cortex, which is normally visual. The precise areas involved and degree of activation are dependent upon the cause and age of onset of blindness. Here, we investigated the cortical language network at rest and during an auditory covert naming task in five bilaterally anophthalmic subjects, who have never received visual input. When listening to auditory definitions and covertly retrieving words, these subjects activated lateral occipital cortex bilaterally in addition to the language areas activated in sighted controls. This activity was significantly greater than that present in a control condition of listening to reversed speech. The lateral occipital cortex was also recruited into a left-lateralized resting-state network that usually comprises anterior and posterior language areas. Levels of activation to the auditory naming and reversed speech conditions did not differ in the calcarine (striate) cortex. This primary 'visual' cortex was not recruited to the left-lateralized resting-state network and showed high interhemispheric correlation of activity at rest, as is typically seen in unimodal cortical areas. In contrast, the interhemispheric correlation of resting activity in extrastriate areas was reduced in anophthalmia to the level of cortical areas that are heteromodal, such as the inferior frontal gyrus. Previous imaging studies in the congenitally blind show that primary visual cortex is activated in higher-order tasks, such as language and memory to a greater extent than during more basic sensory processing, resulting in a reversal of the normal hierarchy of functional organization across 'visual' areas. Our data do not support such a pattern of organization in anophthalmia. Instead, the patterns of activity during task and the functional connectivity at rest are consistent with the known hierarchy of processing in these areas normally seen for vision. The differences in cortical organization between bilateral anophthalmia and other forms of congenital blindness are considered to be due to the total absence of stimulation in 'visual' cortex by light or retinal activity in the former condition, and suggests development of subcortical auditory input to the geniculo-striate pathway.

Occipital Cortex of Blind Individuals Is Functionally Coupled with Executive Control Areas of Frontal Cortex

“…However, we consider this interpretation unlikely. Our study, like prior reports, did not observe increased functional connectivity between occipital cortex and other regions involved in language processing, such as left temporal regions (Watkins et al, 2012;Bedny et al, 2011), suggesting that a role in language processing is not sufficient to increase functional connectivity with occipital areas. Second, we find that increased functional correlations were stable across rest and two different task contexts, suggesting that the observed group differences are robust to substantial variations in ongoing cognitive activity.…”

“…We use a data-driven GDC approach to identify a group of prefrontal areas that has increased connectivity with occipital cortex in congenitally blind individuals (Watkins et al, 2012;Bedny et al, 2011;Liu et al, 2007). The GDC approach provides a more comprehensive picture of occipital functional connectivity in blindness than previously possible.…”

“…We focus on correlations between ipsilateral frontal and occipital cortices, which are thought to be altered in blindness ( Watkins et al, 2012). Specifically, we search for occipital voxels that have group differences in connectivity with a large number of frontal voxels and frontal voxels that have group differences with a large number of occipital voxels.…”

“…Evidence for this comes from studies of resting state functional connectivity MRI (fcMRI), which measures temporal correlations between hemodynamic signals from different brain regions, in the absence of a task (Biswal, Yetkin, Haughton, & Hyde, 1995). Previous fcMRI studies of blind individuals converge on a surprising finding: Rather than increased functional connectivity to nonvisual sensory areas, the occipital cortex of early blind adults shows increased functional connectivity to regions of pFC (Watkins et al, 2012;Bedny et al, 2011;Liu et al, 2007).…”

Evaluation and calibration of functional network modeling methods based on known anatomical connections

“…If the way the two regions vary is related, then they are said to be correlated. Correlati using fMRI data are plentiful and have looked at many things from the modular organization of functional networks in children with frontal lobe epilepsy (Vaessen et al, 2012), to language networks in subjects with anophthalmia (Watkins et al, 2012), to the reliability of the identification of the default mode network (Long et al, 2008). Partial correlation is also a widely used method which seeks to identify direct connections, rather than the direct and the indirect as identified with correlation , by regressing out information from all additional regions in the network in considering the relationship between two regions.…”