Visuo‑spatial Attention And Semantic Memory Competition in The Parietal Cortex

Neuroimaging studies associate specific functional roles to distinct brain regions investigating separate cognitive processes using dedicated tasks. For example, using both correlative (i.e., fMRI) and causal (i.e., TMS) approaches it has been shown the involvement of intra-parietal sulcus (IPS), as part of the dorsal attention network, in spatial attentional tasks as well as the importance of the angular gyrus (AG), as part of the default mode network, during the selection of relevant information in semantic memory.

Neuroimaging technology has gradually become one of the important tools for studying memory. This technique allows us to directly observe changes in brain structure and activity, leading to a better understanding of how memories are generated and stored.

Using neuroimaging techniques, we can see areas of the brain that become active when we learn new content, and these areas gradually change over time. At the same time, we can use this technique to observe how memories stored in our brains are retrieved.

Furthermore, neuroimaging technology can also help us understand the relationship between memory and related diseases. For example, researchers can observe how the brain structure and activity patterns of people with Alzheimer's disease differ from those of normal people, allowing them to better understand how the disease affects memory.

Most importantly, neuroimaging techniques can also support research into new methods of memory enhancement. By observing patterns of brain activity, we can learn what methods have a positive impact on improving memory and explore better memory training methods.

In short, neuroimaging technology provides a powerful tool for us to study memory and related diseases and explore new memory enhancement methods. The development of this technology allows us to better understand and manage our brains, thereby improving our memory and thinking skills. It can be seen that we need to improve memory. Cistanche can significantly improve memory because Cistanche is a traditional Chinese medicinal material with many unique effects, one of which is to improve memory. The efficacy of minced meat comes from the various active ingredients it contains, including acid, polysaccharides, flavonoids, etc. These ingredients can promote brain health in various ways.

Click Know Short-term Memory how to improve

Nonetheless, in our daily life attention and semantic memory are rarely needed in isolation. In the present TMS study,dy we investigate how the brain combines attentional and semantic memory demands in a single task. Results showed that, compared to a pseudo-TMS, stimulation of IPS, but not affect behavioral performance, thus suggesting its preponderant role in such a combined task. Moreover, the lack of difference between the effects of IPS and AG stimulations seems to suggest that the two regions may be coactivated or that a third-party source might indirectly mediate the interaction between the two networks.

In lastest 15 years, a growing body of evidence has shown that the human cerebral cortex can be functionally segregated into a limited set of resting-state networks (RSNs), each composed of several nodes (regions) located in different lobes, which are characterized by coherent spatiotemporal patterns of spontaneous activity. Since these networks are usually studied in resting-state situations, their contribution to psychological states and mental processes has proven difficult to understand, and this network perspective has proven difficult to reconcile with the classical locations view of the cerebral cortex which has dominated cognitive psychology.

In particular, the dichotomy between the so-called “dorsal attention” (DAN) and “default mode” (DMN) networks, characterized by a competitive relationship with each other both at rest and during task performance1, has been often described in psychological terms as controlling external/environmental vs. internal/self-referential processes. For example, neuroimaging studies showed that, within the parietal cortex, the bilateral intraparietal sulcus (IPS), part of the DAN, is involved in visuospatial attention tasks2 Neuron)3,4 . On the contrary, the left angular gyrus (AG, one of the main nodes of the DM5,6, as well as of the language network, is one of the cortical regions mostly engaged in internally oriented tasks8 including semantic9,10 and episodic11 memory.

Such correlative results have been causally confirmed by our group using a causal approach by combining transcranial magnetic stimulation (TMS) electroencephalographyaphy (EEG), showing that both behavioral performance and several local and global EEG markers (e.g., the parietal event-related de-synchronization of the alpha rhythms and the topography of the EEG microstates) were selectively affected when TMS was delivered over the two parietal regions12,13. Specifcally, stimulation of IPS, but not AG, interferes during the execution of a vi visuospatial attention task, whereas stimulation of AG, but not IPS, interferes during a semantic decision task.

However, visual attentional and semantic memory demands ofen occur simultaneously in everyday life. Although there is a large body of research showing the role of IPS and AG in visual attentional and semantic memory, respectively, no study, to our knowledge, has examined how the brain (and the parietal cortex, in particular) combines these two relevant cognitive demands. It remains largely unknown whether IPS and AG contribute differently to a combined attention-memory task. With this point of view, here, by employing alphanumerical contents, we used a single task (see Fig. 1) implying the information processing of both attention and memory to investigate which part of the parietal cortex has a dominant role in such a combined task.

Results

Main analyses

The analyses tested the behavior effects produced by magnetic stimulation over different parietal sites (IPS and AG) during the execution of a combined attention-memory task.

First, we reported a significant main effect of target validity (RTs: valid, 850 ± 21 ms; invalid, 901±23 ms; F(1,17)=52.6, P=0.0001) indicating that subjects effectively allocated attention to a specific location of the visual field. More importantly, we also reportesignificantcant effect ECT of Condition F(2,34)=4.25, P=0.023) indicating a more prominent role of IPS. Indeed, relevant Duncan post hoc tests (P< 0.05) showed that the speed of target discrimination during the IPS stimulation (897 ms±20) was significantly slowed down as compared to Sham (856 ms± 22; P = 0.009) but not as compared to AG stimulation (872 ms± 24; P = 0.09 (Fig. 2B). Moreover, stimulation of AG did not affect behavioral response as compared to Sham (P=0.27). Of note, there was a significant interaction between condition and target validity (P=0.737), suggesting that rTMS did not disrupt the observers’ ability to direct spatial attention to the target location

Te ANOVA on accuracy scores did not reveal any significant effect (p=0.67) indicating a selective interference with the speed of target discrimination.

Furthermore, the analysis to evaluate a possible visufieldeld lateralization showed that the effect of rTMS at different cortical sites was the differentiation of left (ipsilateral) or right (contralateral) misfield field targets (p=0.147). However, targets presented in the right visual field were identified overall more rapidly than targets presented in the lef visual feld (left visual field: 888±9 ms; right visfieldfled: 865±22 ms; F(1,17)=7.1, P=0.016), treflectingting the well-known superiority of the right visual field left hemisphere) for alphabetical material.

Overall, these results suggest that only IPS stimulation interferes with the performance of the present combined attention-memory task.

Control analyses

To control the importance of the present sequential evolution of the cognitive demands in the present combined task, and to distinguish between the effects of TMS on isolated tasks versus their combination in direct comparisons, we compared the current results with that of our previous study12 in which semantic memory and visuospatial attention tasks were tested in isolatioSpecificallylly, we carried out two separate mixed ANOVAs on RTs of correct responses, with Group (Combined, Attention or Memory) between-subject sects variable, and TMS Condition (AG, IPS, Sham) an as a within-subject variable. For both analyses, we reported the main effect of Group (F(1,34) > 89.41, P < 0.001) since in the combined task subjects took longer to respond compared to both attention (p = 0.001) and memory (p = 0.001) isolated tasks. 

Moreover, when we compared the current combined task with the earlier semantic memory task we observed an interaction between Group (Combined, Memory) and TMS Condition (AG, IPS, Sham) F(2,68) = 5.18, P = 0.008), showing that the behavioral performance was significantly impaired following stimulation of IPS as compared to AG (P = 0.049) or Sham (P = 0.002), while the opposite pattern, i.e., higher RTs after stimulation of AG as compared to both IPS (P = 0.014) and Sham (P = 0.003), was observed during the memory task. Notably, this pattern of results is in line with what we found in the previous study comparing attention and memory tasks. On the contrary, when we compared the current combined task with the previous attention task we did not report a statistically significant interaction between Group (Combined, Attention) and TMS Condition (AG, IPS, Sham) F(2,68) = 0.86, P =0.43).

DiscussThen

Te present study examined the causal role of two parietal regions (i.e., IPS and AG) belonging to two distinct brain networks (i.e., DAN and DMN) during the execution of a task combining attentional and semantic memory demand The results indicate that only the inhibition of IPSaffectss the behavioral response, thus suggesting its dominant role in such a combined task.

The link between IPS, as part of the DAN, and visuospatial attention tasks, as well as the link between AG, as part of the DMN, and semantic memory demand, have been widely demonstrated using a correlative approach (i.e., fMRI)3,10. Moreover, previous studies of our group causally confirmed such associations during isolated tasks12,13,16)Specificallyly, only the magnetic stimulation of IPaffectsts behavioral responses during the execution of a visuospatialal attention task, whereas only the stimulation of AG interferes during a semantic decision task12,13.

Environmental and self-referential processes, such as those induced by visual attentional and semantic memory demands, respectively, are rarely needed in isolation in everyday life. How are these two kinds of cognitive demands flexiblely integrated and combined? May the DAN and the DMN directly interact with each other to contribute for example to a combined attention-memory task? The presentation suggests that, compared to a non-active stimulation (i.e., Sham), the behavioral response to a combined attention-memory task was affected only when stimulating the IPS. On the contrary, compared to the Sham condition, the inhibition of AG does not produce interference, despite its well-known role in both semantic memory9 and language7 processes, which are accounted for in the present task. Thiss pattern of results might be explained by the temporal dynamics of the cognitive operations which are engaged to carry out the current task. To accomplish such a combined task, subjects have to first allocate their visuospatial attention and then process the semantic content of the target. 

Therefore, it is likely that magnetic stimulation directly affects the attentional process, hence, it is not surprising to observe a detrimental effect after inhibition of I reflecting the sequential evolution of the cognitive demands. Such a conclusion is also confirmed by a direct comparison between the present results and those of our previous study in which subjects were asked to perform the two tasks (i.e. attention and memory) separately12. In particular when we compared the current combined task with the previous memory task, we reported an interaction similar to what was observed in our referenced study between memory and attention tasks. On the contrary, this interaction was not observed when the current combined task was compared to the previous attention task, thus confirming that the present sequential evolution of the cognitive demands induces stronger impairment when magnetic stimulation is delivered over nodes belonging to the attentional network. With this point of view, we suggest that future TMS studies will deeply corroborate conclusions using experimenparadigmsdigm different timing of stimulation (i.e. before the cue onset and in the period between the cue and the target).

Nevertheless, here we do not report clear differences between IPS and AG, thus suggesting that somehow these regions may have a sort of coactivation in the present combined task. Such coactivation might be characterized by sequential engagement of this parietal region at different time points along the task execution. On the other hand, based on the lack of difference between the inhibition of the two cortical areas, it can be hypothesized the recruitment of a third-party region indirectly mediates the dynamic interplay between DAN and DMNa as a function of task demands Tis view comes from a previous EEG-TMS study in which we investigated the changes in the metrics of the resting EEG microstates, which globally represent transient brain activiafterafer TMS on the IPS and the AG16. In that study, we reported that the focal inhibition of both regions resulted in the modification of topography patterns of an EEG microstate previously associated with the cingulo-opercular network (CON), a separate brain system that is thought to be involved in flexible cognitive control17, thus supporting the hypothesis that the DAN-DMN interaction is indirectly mediated by a higher-order prefrontal network (CON) involved in the maintenance of the task set.

Nonetheless, the involvement of a third-party network in the integration of environmental and self-referential processes is merely an intriguing hypothesis at the present stage, due to the lack of conclusive experiments in the literature. Hence, we suggest that future neuroimaging studies will directly demonstrate the involvement of specific networks in the combination of the two cognitive processes.

Te present fndings may form the basis of successful applications, especially in the field of (neuro)psychological (re)habilitation programs. Patients with focal or diffuse brain damage, as well as patients with developmental disorders, often show behavioral impairments in multiple cognitive domains, as well as difficulties in flexes difficulties cognitive functioning in diverse life situations. This limits the identification of optimal targets for specific cognitive-behavioral treatments or eventually for combined neurostimulation-cognitive approaches. An approach based on dynamic network interactions rather than the role of focal brain regions may develop a new treatment strategy. To conclude, future studies implylso neurophysiological recording will fully shed light on this topic.

Materials and methods

Subjects and Stimuli. right-handed 18ed18 volunteers (mean age±SE=29.8±5.2 years old, 10 females), with no previous psychiatric or neurological history, participated in the experiment. Informed consent was obtained from all participants according to the Code of Ethics of the World Medical Association, and the Institutional Review Board and Ethics Committee of the University of ChiThei. Te method of the present study was carried out with published safety guidelines (see methods section), and the experimental protocol was approved by the Institutional Review Board and Ethics Committee of the University of Chieti. A sensitivity power analysis (GPosoftwareware v. 3.119) revealed that our sample size was large enough to detect meffectsects and interactions of interest with a “smaeffectfect size of 0.18 at an alpha level of p<0.05 with 0.80 power. Of note, this is consistent with commonly used interpretation referring effect sizes as “small” (d=0.2), “medium” (d=0.5), and “large” (d=0.8) based on benchmarks suggested by CohenThe. Te participants were seated on a comfortable reclining armchair and kept their hands on the keyboard. Stimuli were presented on an LCD screen placed at about 80 cm and were generated using E-Prime sofware v2.0 (Psychological Sofware Tools, Pittsburgh, PA), and included four-letter Italian nouns, matched for frequency (mean frequency: 13.4).

Subjects were instructed to maintain fixation on a central black cross (subtending 0.2° of visual angle), displayed on a white background at the center of the screen (Fig. 1). During the experimental task, every 4±0.5 s a cue stimulus (a black arrow subtending about 0.2° visual angle and overlapping with the horizontal segment of the fixation cross) was presented for 200 ms duration, randomly cueing either a lef (50%) or a right (50%) visual field locatiAfterAfer 2 s from cue onset, the target stimulus (word) was presented for 500 ms at either the cued (valid) or the uncued (invalid) location along the horizontal meridian at 0.7° degrees of visual angle fromfixatiThen. Te ratio of valid/invalid targets was 80/2The1. Te subject’s task was to maintain centfixationtion throughout the trial, covertly pay attention to the location indicated by the cue, and make a living/non-living judgment by pressing a corresponding button of the keyboard with the left/right infingerfinger. In this way, subjects performed a semantic judgment during a visuo-spatial task.

Before the experimental sessions, subjects had a long training session (50 trials) to be confident with the task. Then, in each TMS condition, we presented 50 trials (40 valid and 10 invalids), so that a single target word was presented only once during the training session (50 trials) and the three experimental conditions (3 conditions×50 trials=150 trials).

Subjects were instructed to respond as quickly and as accurately as possible. Reaction times and response accuracy were recorded for behavioral analysis.

TMS procedures and identification of target scalp regions.

TMS stimulation was delivered through a focal, figure eight coil, connected with a standard Mag-Stim Rapid 2 stimulator (maximum output 2.2 Tesla). Individual resting excitability threshold for right motor cortex stimulation was preliminarily determined followa ing standardiprocedurerThe2. Te inhibitory rTMS train (i.e., 3 pulses) was delivered simultaneously to the cue onset with the following parameters: 150 ms duration, 20-Hz frequency, and intensity set at 100% of the individual motor threshold. Te parameters are consistent with published safety guidelines for TMS stimulation23. Of note, previous works from our lab have demonstrated the inhibitory nature of the present stimulation protocol12,13,16,24,25.

Each participant performed three conditions, one for each stimulation site, different blocks, whose order was counterbalanced across subjects. In the two experimental conditions, we stimulated over the left AG and IPS, respectively. In the “Sham” condition, a pseudo-RTM was delivered at the scalp vertex; stimulation was ineffective due to the reversed position of the coil concerning the scalp surface (i.e., the magnetic flux was dispersed to air). Notably, this Sham stimulation produces a similar tactile sensation and alerting (sounsomesthesiasic stimulation, etc.) to the active rTThe. Te location of left AG and IPS was automaticallidentifieded on the subject’s scalp using the SofTaxic navigator system (E.M.S. Italy, www.emsmedical.net), which uses a set of digitized skull landmarks (nasion, inion, and two pre-auricular points), and about 40 scalp points entered with a Fastrak Polhemus digitizer system (Polhemus), and an averaged stereotaxic MRI atlas brain in Talairach space. Te average Talairach coordinates in the SofTaxic navigator system were transformed through a linear transformation to each subject’s scalp. Such a method has an error of about 5 mm over a method in which each subject’s own MRI is used for localizationThis Tis strategy has been successful in previous rTMS studies12,24,25,28,29. A mechanical arm maintained the handle of the coil angled at about 45° away from the midline and a centimeter of the coil wings was positioned on the scalp, to deliver the maximum rTMS intensity over each site (individual peak of activatioThe. Te coordinates of the two cortical areas were based on the previous fMRI study assessing task-evoked activity during spatial attention and semantic memory and were as follows: (i) a region of the DAN: lef IPS14; (ii) a region of the DMN: lef AG10 (Fig. 2A).

Statistical analyses.

Statistical analyses were conducted using within-subject ANOVAs for repeated measures. Mauchley’s test was used to evaluate the sphericity assumption n, the Greenhouse–Geisser procedure for correcting the degrees of freedom, and the end Duncteststs for post hoc comparisons (p<0.05).

We used RTs of correct responses or percentage of correct responses (Hits) as dependent variables, and TMS Condition (AG, IPS, Sham) and Validity (Valid, Invalid) as within-subjectject factors. Moreover, to test for potential or interaction between visuafieldld and brain area stimulated, we used RTs of correct responses as dependent variables and TMS Condition (AG, IPS, Sham) and Visuafieldld (target stimulus on the right left side of the screen) as the within-subject factors.

Data availability

Te datasets used during the current story are available from the corresponding author on reasonable request.

References

1. Fox, M. D., Corbetta, M., Snyder, A. Z., Vincent, J. L. & Raichle, M. E. Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. Proc. Natl. Acad. Sci. U S A 103, 10046–10051 (2005). 

2. Corbetta, M. et al. A common network of functional areas for attention and eye movements. Neuron 21(4), 761–773 (1998). 

3. Corbetta, M. & Shulman, G. L. Control of goal-directed stimulus-driveniven attention in the brain. Nat. Rev. Neurosci. 3, 201–215 (2002). 

4. Silver, M. A. & Kastner, S. Topographic maps in human frontal and parietal cortex. Trends Cogn. Sci. 13(11), 488–495 (2009). 

5. Shulman G. L. et al. Common blood flow changes across visual tasks: II. Decreases in cerebral cortex. J. Cogn. Neurosci. 9, 648–663 (1997). 

6. Raichle, M. E. et al. Inaugural article: A default mode of brain function. Proc. Natl. Acad. Sci. USA 98, 676–682 (2001). 

7. Uddin, L. Q. et al. Dissociable connectivity within human angular gyrus and intraparietal sulcus: Evidence from functional and structural connectivity. Cereb. Cortex. 20(11), 2636–2646 (2010). 

8. Buckner, R. L., Andrews-Hanna, J. R. & Schacter, D D. The brain’s default network. Ann. N. Y. Acad. Sci. 1124, 1–38 (2008). 

9. Binder, J. R. & Desai, R. H. Te neurobiology of semantic memory. Trends Cogn. Sci. 15, 527–536 (2011). 

10. Wirth, M. et al. Semantic memory involvement in the default mode network: A functional neuroimaging study using independent component analysis. Neuroimage 54, 3057–3066 (2011). 

11. Sestieri, C., Shulman, G. L. & Corbetta, M. Attention to memory and the environment: functional specialization and dynamic competition in human posterior parietal cortex. J. Neurosci. 30, 8445–8456 (2010). 

12. Capotosto, P. et al. Task and regiospecificifc top-down modulation of alpha rhythms in parietal cortex. Cereb. Cortex. 27(10), 4815–4822 (2017). 

13. Croce, P., Zappasodi, F., Sara, S. & Capotosto, P. Magnetic stimulation selectivaffectsects pre-stimulus EEG microstates. Neuroimage 176, 239–245 (2018). 

14. He, B. J., Snyder, A. Z., Vincent, J. L., Epstein, A., Shulman, G. L. & Corbetta, M. Breakdown of functional connectivity in frontoparietal networks underlies behavioral deficits in spatial neglect. Neuron 53, 905–918 (2007). 

15. Rizzolatti, G., Umiltà, C. & Berlucchi, G. Opposite superiorities of the right-left left cerebral hemispheres in discriminative reaction time to physiognomical and alphabetical material. Brain 94(3), 431–442 (1971).

For more information:1950477648nn@gmail.com