RESUMO
We continually shift our attention between items in the visual environment. These attention shifts are usually based on task relevance (top-down) or the saliency of a sudden, unexpected stimulus (bottom-up), and are typically followed by goal-directed actions. It could be argued that any species that can covertly shift its focus of attention will rely on similar, evolutionarily conserved neural substrates for processing such shift-signals. To address this possibility, we performed comparative fMRI experiments in humans and monkeys, combining traditional, and novel, data-driven analytical approaches. Specifically, we examined correspondences between monkey and human brain areas activated during covert attention shifts. When "shift" events were compared with "stay" events, the medial (superior) parietal lobe (mSPL) and inferior parietal lobes showed similar shift sensitivities across species, whereas frontal activations were stronger in monkeys. To identify, in a data-driven manner, monkey regions that corresponded with human shift-selective SPL, we used a novel interspecies beta-correlation strategy whereby task-related beta-values were correlated across voxels or regions-of-interest in the 2 species. Monkey medial parietal areas V6/V6A most consistently correlated with shift-selective human mSPL. Our results indicate that both species recruit corresponding, evolutionarily conserved regions within the medial superior parietal lobe for shifting spatial attention.
Assuntos
Atenção/fisiologia , Lobo Parietal/fisiologia , Adulto , Animais , Mapeamento Encefálico , Feminino , Humanos , Macaca mulatta , Imageamento por Ressonância Magnética , Masculino , Estimulação Luminosa , Adulto JovemRESUMO
A unifying function associated with the default mode network (DMN), which is more active during rest than under active task conditions, has been difficult to define. The DMN is activated during monitoring the external world for unexpected events, as a sentinel, and when humans are engaged in high-level internally focused tasks. The existence of DMN correlates in other species, such as mice, challenge the idea that internally focused, high-level cognitive operations, such as introspection, autobiographical memory retrieval, planning the future, and predicting someone else's thoughts, are evolutionarily preserved defining properties of the DMN. A recent human study demonstrated that demanding cognitive shifts could recruit the DMN, yet it is unknown whether this holds for nonhuman species. Therefore, we tested whether large changes in cognitive context would recruit DMN regions in female and male nonhuman primates. Such changes were measured as displacements of spatial attentional weights based on internal rules of relevance (spatial shifts) compared with maintaining attentional weights at the same location (stay events). Using fMRI in macaques, we detected that a cortical network, activated during shifts, largely overlapped with the DMN. Moreover, fMRI time courses sampled from independently defined DMN foci showed significant shift selectivity during the demanding attention task. Finally, functional clustering based on independent resting state data revealed that DMN and shift regions clustered conjointly, whereas regions activated during the stay events clustered apart. We therefore propose that cognitive shifting in primates generally recruits DMN regions. This might explain a breakdown of the DMN in many neurological diseases characterized by declined cognitive flexibility.SIGNIFICANCE STATEMENT Activation of the human default mode network (DMN) can be measured with fMRI when subjects shift thoughts between high-level internally directed cognitive states, when thinking about the self, the perspective of others, when imagining future and past events, and during mind wandering. Furthermore, the DMN is activated as a sentinel, monitoring the environment for unexpected events. Arguably, these cognitive processes have in common fast and substantial changes in cognitive context. As DMN activity has also been reported in nonhuman species, we tested whether shifts in spatial attention activated the monkey DMN. Core monkey DMN and shift-selective regions shared several functional properties, indicating that cognitive shifting, in general, might constitute one of the evolutionarily preserved functions of the DMN.
Assuntos
Atenção/fisiologia , Rede Nervosa/fisiologia , Recrutamento Neurofisiológico/fisiologia , Animais , Mapeamento Encefálico , Cognição/fisiologia , Feminino , Lateralidade Funcional/fisiologia , Macaca mulatta , Imageamento por Ressonância Magnética , Masculino , Estimulação Luminosa , Análise de Componente Principal , Percepção Espacial/fisiologiaRESUMO
In the awake state, shifts of spatial attention alternate with periods of sustained attention at a fixed location or object. Human fMRI experiments revealed the critical role of the superior parietal lobule (SPL) in shifting spatial attention, a finding not predicted by human lesion studies and monkey electrophysiology. To investigate whether a potential homolog of the human SPL shifting region exists in monkeys (Macaca mulatta), we adopted an event-related fMRI paradigm that closely resembled a human experiment (Molenberghs et al., 2007). In this paradigm, a pair of relevant and irrelevant shapes was continuously present on the horizontal meridian. Subjects had to covertly detect a dimming of the relevant shape while ignoring the irrelevant dimmings. The events of interest consisted of the replacement of one stimulus pair by the next. During shift but not stay events, the relevant shape of the new pair appeared at the contralateral position relative to the previous one. Spatial shifting events activated parietal areas V6/V6A and medial intraparietal area, caudo-dorsal visual areas, the most posterior portion of the superior temporal sulcus, and several smaller frontal areas. These areas were not activated during passive stimulation with the same sensory stimuli. During stay events, strong direction-sensitive attention signals were observed in a distributed set of contralateral visual, temporal, parietal, and lateral prefrontal areas, the vast majority overlapping with the sensory stimulus representation. We suggest medial intraparietal area and V6/V6A as functional counterparts of human SPL because they contained the most widespread shift signals in the absence of contralateral stay activity, resembling the functional characteristics of the human SPL shifting area.
Assuntos
Atenção , Conectoma , Lobo Parietal/fisiologia , Percepção Espacial , Córtex Visual/fisiologia , Animais , Feminino , Macaca mulatta , MasculinoRESUMO
Neurophysiological and functional imaging studies have investigated the representation of animate and inanimate stimulus classes in monkey inferior temporal (IT) and human occipito-temporal cortex (OTC). These studies proposed a distributed representation of stimulus categories across IT and OTC and at the same time highlighted category specific modules for the processing of bodies, faces and objects. Here, we investigated whether the stimulus representation within the extrastriate (EBA) and the fusiform (FBA) body areas differed from the representation across OTC. To address this question, we performed an event-related fMRI experiment, evaluating the pattern of activation elicited by 200 individual stimuli that had already been extensively tested in our earlier monkey imaging and single cell studies (Popivanov et al., 2012, 2014). The set contained achromatic images of headless monkey and human bodies, two sets of man-made objects, monkey and human faces, four-legged mammals, birds, fruits, and sculptures. The fMRI response patterns within EBA and FBA primarily distinguished bodies from non-body stimuli, with subtle differences between the areas. However, despite responding on average stronger to bodies than to other categories, classification performance for preferred and non-preferred categories was comparable. OTC primarily distinguished animate from inanimate stimuli. However, cluster analysis revealed a much more fine-grained representation with several homogeneous clusters consisting entirely of stimuli of individual categories. Overall, our data suggest that category representation varies with location within OTC. Nevertheless, body modules contain information to discriminate also non-preferred stimuli and show an increasing specificity in a posterior to anterior gradient.
Assuntos
Lobo Occipital/fisiologia , Reconhecimento Visual de Modelos/fisiologia , Lobo Temporal/fisiologia , Adulto , Mapeamento Encefálico , Potenciais Evocados Visuais , Face , Feminino , Humanos , Imageamento por Ressonância Magnética , Masculino , Estimulação Luminosa , Tronco , Adulto JovemRESUMO
The intraparietal sulcus (IPS) is critical for resolving stimulus competition. Its activity is modulated depending on how competing stimuli are spatially configured. Lesions extending into IPS lead to selection deficits when stimuli are configured along a horizontal relative to a vertical or diagonal axis. Using functional magnetic resonance imaging, we examined whether the effect of configuration axis originates at the level of the sensory map in early visual cortex or at the level of the attentional priority map in IPS. In each trial, we presented 1 or 2 peripheral gratings in the upper right visual field and a central letter stream. Subjects performed either a peripheral orientation discrimination task or a central letter detection task. Left IPS activity was higher when peripheral stimuli were configured along the horizontal relative to the vertical axis, but only in peripheral attention conditions. The portions of extrastriate cortex that responded to the peripheral stimuli showed a similar interaction. Connectivity from superior parietal to extrastriate cortex was enhanced by adding a competing distracter during the peripheral attention task. The effect of the spatial configuration between competing stimuli originates at the level of the attentional priority map in IPS rather than the visual sensory map.