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Neocortical-hippocampal dynamics of working memory in healthy and diseased brain states based on functional connectivity.

Poch C, Campo P - Front Hum Neurosci (2012)

Bottom Line: Recent findings demonstrate that WM abilities are not determined solely by local brain activity, but also rely on the functional coupling of neocortical-hippocampal regions to support WM processes.Although the hippocampus has long been held to be important for long-term declarative memory, recent evidence suggests that the hippocampus may also be necessary to coordinate disparate cortical regions supporting the periodic reactivation of internal representations in WM.Furthermore, recent brain imaging studies using connectivity measures, have shown that changes in cortico-limbic interactions can be useful to characterize WM impairments observed in different neuropathological conditions.

View Article: PubMed Central - PubMed

Affiliation: Center for Biomedical Technology, Laboratory of Cognitive and Computatioal Neuroscience, Complutense University of Madrid, Polytechnic University of Madrid Madrid, Spain.

ABSTRACT
Working memory (WM) is the ability to transiently maintain and manipulate internal representations beyond its external availability to the senses. This process is thought to support high level cognitive abilities and been shown to be strongly predictive of individual intelligence and reasoning abilities. While early models of WM have relied on a modular perspective of brain functioning, more recent evidence suggests that cognitive functions emerge from the interactions of multiple brain regions to generate large-scale networks. Here we will review the current research on functional connectivity of WM processes to highlight the critical role played by neural interactions in healthy and pathological brain states. Recent findings demonstrate that WM abilities are not determined solely by local brain activity, but also rely on the functional coupling of neocortical-hippocampal regions to support WM processes. Although the hippocampus has long been held to be important for long-term declarative memory, recent evidence suggests that the hippocampus may also be necessary to coordinate disparate cortical regions supporting the periodic reactivation of internal representations in WM. Furthermore, recent brain imaging studies using connectivity measures, have shown that changes in cortico-limbic interactions can be useful to characterize WM impairments observed in different neuropathological conditions. Recent advances in electrophysiological and neuroimaging techniques to model network activity has led to important insights into how neocortical and hippocampal regions support WM processes and how disruptions along this network can lead to the memory impairments commonly reported in many neuropathological populations.

No MeSH data available.


Related in: MedlinePlus

Unitary memory models and associated functional connectivity networks. (A) Unitary memory models posit that perception, WM and LTM do not differ in the underlying neural substrates, but in the state of information representations. Accordingly, two or three states are proposed: a focused of attention (FA); a region of direct access (DA); and other information that is hypothesized to be an activated portion of LTM (aLTM). The last two states are considered to be undistinguishable by some authors leading to two states models (Oberauer, 2002; McElree, 2006; Lustig et al., 2009; Öztekin et al., 2010; Nee and Jonides, 2011). (B) Serial position task (SP) of 12 items used to explore differences among the three hypothesized states, and to investigate underlying neural networks. SP12 corresponds to FA; SP9–11 corresponds to DA; SP1–8 corresponds to aLTM [Adapted from (Öztekin et al., 2010)]. (C) Regions demonstrating functional connectivity increases with right ITG related to the focus of attention [Adapted from Nee and Jonides (2008)]. (D) Some of the regions demonstrating enhanced connectivity with left mid-VLPFC related to aLTM [Adapted from Nee and Jonides (2008)]. Other regions were anterior STG and ventromedial PFC. ITG, inferior temporal gyrus; MTL, medial temporal lobe; OC, occipital cortex; PPC, posterior parietal cortex; STG, superior temporal gyrus; VLPFC, ventrolateral prefrontal cortex.
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Figure 1: Unitary memory models and associated functional connectivity networks. (A) Unitary memory models posit that perception, WM and LTM do not differ in the underlying neural substrates, but in the state of information representations. Accordingly, two or three states are proposed: a focused of attention (FA); a region of direct access (DA); and other information that is hypothesized to be an activated portion of LTM (aLTM). The last two states are considered to be undistinguishable by some authors leading to two states models (Oberauer, 2002; McElree, 2006; Lustig et al., 2009; Öztekin et al., 2010; Nee and Jonides, 2011). (B) Serial position task (SP) of 12 items used to explore differences among the three hypothesized states, and to investigate underlying neural networks. SP12 corresponds to FA; SP9–11 corresponds to DA; SP1–8 corresponds to aLTM [Adapted from (Öztekin et al., 2010)]. (C) Regions demonstrating functional connectivity increases with right ITG related to the focus of attention [Adapted from Nee and Jonides (2008)]. (D) Some of the regions demonstrating enhanced connectivity with left mid-VLPFC related to aLTM [Adapted from Nee and Jonides (2008)]. Other regions were anterior STG and ventromedial PFC. ITG, inferior temporal gyrus; MTL, medial temporal lobe; OC, occipital cortex; PPC, posterior parietal cortex; STG, superior temporal gyrus; VLPFC, ventrolateral prefrontal cortex.

Mentions: We have seen a number of studies showing that WM depends on a neural network including PFC, MTL, and posterior neocortical regions, whose interactions are modified to accommodate the increase of mnemonic demands. Similar functional networks have been described for studies exploring patterns of connectivity during LTM processes (Rajah et al., 1999; Fell et al., 2001; Simons and Spiers, 2003; Addis and McAndrews, 2006; Summerfield et al., 2006; Kahn et al., 2008; Babiloni et al., 2009; Anderson et al., 2010). These evidences constitute further support for the emerging view that the hippocampus and related structures form part of a neural network involved in both LTM and WM processes. However, despite the similarity between neural networks, the question emerges as to whether the connectivity among the elements of these apparently analogous functional networks differ qualitatively or quantitatively, thus allowing for a distinction between memory processes (McIntosh, 1999; Rajah and McIntosh, 2005). Accordingly, direct examinations of the pattern of interactions of MTL across tasks simultaneously tapping both WM and LTM process are needed in order to determine whether these interactions are reflecting a common functional architecture or not (Axmacher et al., 2009a; Fell and Axmacher, 2011). Using tasks designed under the influence of the framework of unitary memory systems (Cowan, 2001; Oberauer, 2002; McElree, 2006) could shed light on this question (see Figure 1). These models consider that information could be represented in different states, either in the focus of attention or in an activated state with different accessibility (Lustig et al., 2009; Nee and Jonides, 2011). Whether neural networks underlying these states were similar or could be differentiated was investigated in a recent fMRI study (Nee and Jonides, 2008). In this study mechanisms of retrieval of items within the focus of attention or outside the focus (i.e., WM) were explored using functional connectivity analyses. Information considered to be within the focus of attention was associated with stronger connectivity between ITC and frontal and posterior parietal regions (see also Roth and Courtney, 2007). Crucially, retrieval dynamics of information outside the focus (Lewis-Peacock et al., 2012) were characterized by increased coupling between ventrolateral prefrontal cortex (VLPFC) and MTL, as well as with other neocortical sites, as a function of retrieval demands (see Figure 1). Results from Rissman et al. (2008), can be interpreted under this framework. While increased PFC-ITC coupling was observed during maintenance of low WM load (i.e., one face), increased involvement of MTL and PFC mediated coupling was observed at higher mnemonic loads (i.e., four faces). Hence, these data support that processes of STM are similar to those implicated in LTM, suggesting common underlying mechanisms between STM and LTM. Nonetheless, differentiation between retrieval and updating of information should be explored in order to refine the characterization of the neural bases reported by this study (Bledowski et al., 2009; although see Roth and Courtney, 2007). Additionally, whether the information outside the focus of attention is better explained by two-state models or by three-state models are in need of further functional connectivity studies (Öztekin et al., 2010; Lewis-Peacock et al., 2012; Nee and Jonides, 2011).


Neocortical-hippocampal dynamics of working memory in healthy and diseased brain states based on functional connectivity.

Poch C, Campo P - Front Hum Neurosci (2012)

Unitary memory models and associated functional connectivity networks. (A) Unitary memory models posit that perception, WM and LTM do not differ in the underlying neural substrates, but in the state of information representations. Accordingly, two or three states are proposed: a focused of attention (FA); a region of direct access (DA); and other information that is hypothesized to be an activated portion of LTM (aLTM). The last two states are considered to be undistinguishable by some authors leading to two states models (Oberauer, 2002; McElree, 2006; Lustig et al., 2009; Öztekin et al., 2010; Nee and Jonides, 2011). (B) Serial position task (SP) of 12 items used to explore differences among the three hypothesized states, and to investigate underlying neural networks. SP12 corresponds to FA; SP9–11 corresponds to DA; SP1–8 corresponds to aLTM [Adapted from (Öztekin et al., 2010)]. (C) Regions demonstrating functional connectivity increases with right ITG related to the focus of attention [Adapted from Nee and Jonides (2008)]. (D) Some of the regions demonstrating enhanced connectivity with left mid-VLPFC related to aLTM [Adapted from Nee and Jonides (2008)]. Other regions were anterior STG and ventromedial PFC. ITG, inferior temporal gyrus; MTL, medial temporal lobe; OC, occipital cortex; PPC, posterior parietal cortex; STG, superior temporal gyrus; VLPFC, ventrolateral prefrontal cortex.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3293391&req=5

Figure 1: Unitary memory models and associated functional connectivity networks. (A) Unitary memory models posit that perception, WM and LTM do not differ in the underlying neural substrates, but in the state of information representations. Accordingly, two or three states are proposed: a focused of attention (FA); a region of direct access (DA); and other information that is hypothesized to be an activated portion of LTM (aLTM). The last two states are considered to be undistinguishable by some authors leading to two states models (Oberauer, 2002; McElree, 2006; Lustig et al., 2009; Öztekin et al., 2010; Nee and Jonides, 2011). (B) Serial position task (SP) of 12 items used to explore differences among the three hypothesized states, and to investigate underlying neural networks. SP12 corresponds to FA; SP9–11 corresponds to DA; SP1–8 corresponds to aLTM [Adapted from (Öztekin et al., 2010)]. (C) Regions demonstrating functional connectivity increases with right ITG related to the focus of attention [Adapted from Nee and Jonides (2008)]. (D) Some of the regions demonstrating enhanced connectivity with left mid-VLPFC related to aLTM [Adapted from Nee and Jonides (2008)]. Other regions were anterior STG and ventromedial PFC. ITG, inferior temporal gyrus; MTL, medial temporal lobe; OC, occipital cortex; PPC, posterior parietal cortex; STG, superior temporal gyrus; VLPFC, ventrolateral prefrontal cortex.
Mentions: We have seen a number of studies showing that WM depends on a neural network including PFC, MTL, and posterior neocortical regions, whose interactions are modified to accommodate the increase of mnemonic demands. Similar functional networks have been described for studies exploring patterns of connectivity during LTM processes (Rajah et al., 1999; Fell et al., 2001; Simons and Spiers, 2003; Addis and McAndrews, 2006; Summerfield et al., 2006; Kahn et al., 2008; Babiloni et al., 2009; Anderson et al., 2010). These evidences constitute further support for the emerging view that the hippocampus and related structures form part of a neural network involved in both LTM and WM processes. However, despite the similarity between neural networks, the question emerges as to whether the connectivity among the elements of these apparently analogous functional networks differ qualitatively or quantitatively, thus allowing for a distinction between memory processes (McIntosh, 1999; Rajah and McIntosh, 2005). Accordingly, direct examinations of the pattern of interactions of MTL across tasks simultaneously tapping both WM and LTM process are needed in order to determine whether these interactions are reflecting a common functional architecture or not (Axmacher et al., 2009a; Fell and Axmacher, 2011). Using tasks designed under the influence of the framework of unitary memory systems (Cowan, 2001; Oberauer, 2002; McElree, 2006) could shed light on this question (see Figure 1). These models consider that information could be represented in different states, either in the focus of attention or in an activated state with different accessibility (Lustig et al., 2009; Nee and Jonides, 2011). Whether neural networks underlying these states were similar or could be differentiated was investigated in a recent fMRI study (Nee and Jonides, 2008). In this study mechanisms of retrieval of items within the focus of attention or outside the focus (i.e., WM) were explored using functional connectivity analyses. Information considered to be within the focus of attention was associated with stronger connectivity between ITC and frontal and posterior parietal regions (see also Roth and Courtney, 2007). Crucially, retrieval dynamics of information outside the focus (Lewis-Peacock et al., 2012) were characterized by increased coupling between ventrolateral prefrontal cortex (VLPFC) and MTL, as well as with other neocortical sites, as a function of retrieval demands (see Figure 1). Results from Rissman et al. (2008), can be interpreted under this framework. While increased PFC-ITC coupling was observed during maintenance of low WM load (i.e., one face), increased involvement of MTL and PFC mediated coupling was observed at higher mnemonic loads (i.e., four faces). Hence, these data support that processes of STM are similar to those implicated in LTM, suggesting common underlying mechanisms between STM and LTM. Nonetheless, differentiation between retrieval and updating of information should be explored in order to refine the characterization of the neural bases reported by this study (Bledowski et al., 2009; although see Roth and Courtney, 2007). Additionally, whether the information outside the focus of attention is better explained by two-state models or by three-state models are in need of further functional connectivity studies (Öztekin et al., 2010; Lewis-Peacock et al., 2012; Nee and Jonides, 2011).

Bottom Line: Recent findings demonstrate that WM abilities are not determined solely by local brain activity, but also rely on the functional coupling of neocortical-hippocampal regions to support WM processes.Although the hippocampus has long been held to be important for long-term declarative memory, recent evidence suggests that the hippocampus may also be necessary to coordinate disparate cortical regions supporting the periodic reactivation of internal representations in WM.Furthermore, recent brain imaging studies using connectivity measures, have shown that changes in cortico-limbic interactions can be useful to characterize WM impairments observed in different neuropathological conditions.

View Article: PubMed Central - PubMed

Affiliation: Center for Biomedical Technology, Laboratory of Cognitive and Computatioal Neuroscience, Complutense University of Madrid, Polytechnic University of Madrid Madrid, Spain.

ABSTRACT
Working memory (WM) is the ability to transiently maintain and manipulate internal representations beyond its external availability to the senses. This process is thought to support high level cognitive abilities and been shown to be strongly predictive of individual intelligence and reasoning abilities. While early models of WM have relied on a modular perspective of brain functioning, more recent evidence suggests that cognitive functions emerge from the interactions of multiple brain regions to generate large-scale networks. Here we will review the current research on functional connectivity of WM processes to highlight the critical role played by neural interactions in healthy and pathological brain states. Recent findings demonstrate that WM abilities are not determined solely by local brain activity, but also rely on the functional coupling of neocortical-hippocampal regions to support WM processes. Although the hippocampus has long been held to be important for long-term declarative memory, recent evidence suggests that the hippocampus may also be necessary to coordinate disparate cortical regions supporting the periodic reactivation of internal representations in WM. Furthermore, recent brain imaging studies using connectivity measures, have shown that changes in cortico-limbic interactions can be useful to characterize WM impairments observed in different neuropathological conditions. Recent advances in electrophysiological and neuroimaging techniques to model network activity has led to important insights into how neocortical and hippocampal regions support WM processes and how disruptions along this network can lead to the memory impairments commonly reported in many neuropathological populations.

No MeSH data available.


Related in: MedlinePlus