Differences in Intrinsic Functional Organization Between Dorsolateral Prefrontal and Posterior Parietal Cortex

Department of Neurobiology and Anatomy, Wake Forest University School of Medicine, Winston-Salem, NC 27157, USA.
Cerebral Cortex (Impact Factor: 8.67). 03/2013; 24(9). DOI: 10.1093/cercor/bht087
Source: PubMed


The dorsolateral prefrontal and posterior parietal cortex are 2 components of the cortical network controlling attention,
working memory, and executive function. Little is known about how the anatomical organization of the 2 areas accounts for
their functional specialization. In order to address this question, we examined the strength of intrinsic functional connectivity
between neurons sampled in each area by means of cross-correlation analyses of simultaneous recordings from monkeys trained
to perform working memory tasks. In both areas, effective connectivity declined as a function of distance between neurons.
However, the strength of effective connectivity was higher overall and more localized over short distances in the posterior
parietal than the prefrontal cortex. The difference in connectivity strength between the 2 areas could not be explained by
differences in firing rate or selectivity for the stimuli and task events, it was present when the fixation period alone was
analyzed, and according to simulation results, was consistent with a systematic difference either in the strength or in the
relative numbers of shared inputs between neurons. Our results indicate that the 2 areas are characterized by unique intrinsic
functional organization, consistent with known differences in their response patterns during working memory.


Available from: Emilio Salinas, Mar 26, 2014
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    • "The link between tuning and spike time synchrony in IT is controversial, with some evidence that neurons that are similarly tuned are also synchronized (Tamura et al. 2004) and other evidence suggesting no link (Aggelopoulos et al. 2005; Gawne and Richmond 1993; Gochin et al. 1991). A possible explanation for these differing results is that tuning and spike time synchrony may share a common functional structure in which most nearby neurons are weakly correlated in tuning and spike timing, but some neurons have more similar tuning and stronger synchrony, as our laboratory and others have found in retina and multiple cortical areas (Chu et al. 2014; Fukushima et al. 2012; Harris et al. 2003; Katsuki et al. 2013; Stevenson et al. 2012). Also, investigation during muscle relaxation (Tamura et al. 2004) has the advantage of avoiding eye movement-related synchrony that may obscure the underlying structure (Ito et al. 2011; Rajkai et al. 2008). "
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    ABSTRACT: Investigating the relationship between tuning and spike timing is necessary to understand how neuronal populations in anterior visual cortex process complex stimuli. Are tuning and spontaneous spike time synchrony linked by a common spatial structure (do some cells co- vary more strongly, even in the absence of visual stimulation?), and what is the object coding capability of this structure? Here, we recorded from spiking populations in macaque inferior temporal (IT) cortex under neurolept anesthesia. We report that although most nearby IT neurons are weakly correlated, neurons with more similar tuning are also more synchronized during spontaneous activity. This link between tuning and synchrony was not simply due to cell separation distance. Instead, it expands on previous reports that neurons along an IT penetration are tuned to similar but slightly different features. This constraint on possible population firing rate patterns was consistent across stimulus sets, including animate versus inanimate object categories. A classifier trained on this structure was able to generalize category 'read-out' to untrained objects using only a few dimensions (a few patterns of site weightings per electrode array). We suggest that tuning and spike synchrony are linked by a common spatial structure that is highly efficient for object representation.
    Journal of Neurophysiology 05/2014; 112(4). DOI:10.1152/jn.00485.2013 · 2.89 Impact Factor
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    • "Previous studies in different cortical areas demonstrated that strength of effective connectivity declined systematically as a function of horizontal distance between two neurons [43]–[45]. We reported in a prior study that the intrinsic effective connectivity of PPC neurons was higher than dlPFC neurons during the working memory tasks, particularly for the pairs with short (≤0.3 mm) horizontal distances between neurons [31]. Lower effective connectivity in the dlPFC during the delay period might have been observed due to unequally distributed distances in the two samples. "
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    ABSTRACT: The dorsolateral prefrontal and posterior parietal cortex play critical roles in mediating attention, working memory, and executive function. Despite proposed dynamic modulation of connectivity strength within each area according to task demands, scant empirical data exist about the time course of the strength of effective connectivity, particularly in tasks requiring information to be sustained in working memory. We investigated this question by performing time-resolved cross-correlation analysis for pairs of neurons recorded simultaneously at distances of 0.2-1.5 mm apart of each other while monkeys were engaged in working memory tasks. The strength of effective connectivity determined in this manner was higher throughout the trial in the posterior parietal cortex than the dorsolateral prefrontal cortex. Significantly higher levels of parietal effective connectivity were observed specifically during the delay period of the task. These differences could not be accounted for by differences in firing rate, or electrode distance in the samples recorded in the posterior parietal and prefrontal cortex. Differences were present when we restricted our analysis to only neurons with significant delay period activity and overlapping receptive fields. Our results indicate that dynamic changes in connectivity strength are present but area-specific intrinsic organization is the predominant factor that determines the strength of connections between neurons in each of the two areas.
    PLoS ONE 11/2013; 8(11):e81601. DOI:10.1371/journal.pone.0081601 · 3.23 Impact Factor
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    ABSTRACT: The prefrontal cortex continues to mature after puberty and into early adulthood, mirroring the time course of maturation of cognitive abilities. However, the way in which prefrontal activity changes during peri- and postpubertal cortical maturation is largely unknown. To address this question, we evaluated the developmental stage of peripubertal rhesus monkeys with a series of morphometric, hormonal, and radiographic measures, and conducted behavioral and neurophysiological tests as the monkeys performed working memory tasks. We compared firing rate and the strength of intrinsic functional connectivity between neurons in peripubertal vs. adult monkeys. Notably, analyses of spike train cross-correlations demonstrated that the average magnitude of functional connections measured between neurons was lower overall in the prefrontal cortex of peripubertal monkeys compared with adults. The difference resulted because negative functional connections (indicative of inhibitory interactions) were stronger and more prevalent in peripubertal compared with adult monkeys, whereas the positive connections showed similar distributions in the two groups. Our results identify changes in the intrinsic connectivity of prefrontal neurons, particularly that mediated by inhibition, as a possible substrate for peri- and postpubertal advances in cognitive capacity.
    Proceedings of the National Academy of Sciences 02/2014; 111(10). DOI:10.1073/pnas.1316594111 · 9.67 Impact Factor
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