Elsevier

NeuroImage

Volume 29, Issue 4, 15 February 2006, Pages 1185-1191
NeuroImage

Interrupting the “stream of consciousness”: An fMRI investigation

https://doi.org/10.1016/j.neuroimage.2005.09.030Get rights and content

Abstract

In functional neuroimaging, a local decrease in blood flow during an active task, relative to a “resting” baseline, is referred to as task-induced deactivation (TID). TID may occur when resources shift from ongoing, internally generated processing typical of “resting” states to processing required by an exogenous task. We previously found specific brain regions in which TID increased as task processing demands increased. When engaged in an exogenous cognitive task, reallocation of resources from areas involved in internal processing should result in suspension of that processing. Self-reported thought content has been used as an indicator of the extent of internal processing activity. We investigated the relationship between TID and task-unrelated thought (TUT) frequency using an auditory target detection task with seven levels of task difficulty. At varied intervals during task performance, subjects indicated whether they were experiencing a TUT. We expected TUT frequency to decrease as task demands increased and for this pattern to correlate with TID magnitude across conditions. Generally, fewer TUTs were reported during difficult task conditions than during easier conditions. As TID magnitude increased across task conditions, the frequency of TUTs declined (r = 0.90, P = 0.005). Four left hemisphere regions (posterior parieto-occipital cortex, anterior cingulate gyrus, fusiform gyrus, and middle frontal gyrus) showed strong relationships between TUTs and TID (r > 0.79, P < 0.05 corrected). As these regions have been implicated in semantic processing and self-referential thought, the findings support the suspension of internal cognitive processing as one mechanism for TID.

Introduction

Researchers studying brain function generally assume that presentation of a stimulus or task will induce increased neural activity in the brain relative to a resting state. Investigators using functional neuroimaging techniques to study human cognition have been surprised to find that many tasks also produce relative decreases in blood flow or blood-oxygenation indexes of neural activity, a phenomenon referred to as “task-induced deactivation” (TID). Several studies (Binder et al., 1999, Mazoyer et al., 2001, McKiernan et al., 2003, Shulman et al., 1997) demonstrated that TID occurs consistently in specific brain regions, including posterior cingulate cortex, dorsomedial prefrontal cortex, rostral anterior cingulate gyrus, orbitofrontal cortex, and angular gyrus. The mechanisms underlying these deactivations, however, are not fully understood.

Some researchers (Binder et al., 1999, Gusnard and Raichle, 2001, Mazoyer et al., 2001, McKiernan et al., 2003, Raichle et al., 2001, Shulman et al., 1997) have speculated that the “resting” condition is actually a state of organized cognitive activity involving many processes, including monitoring of the external environment, monitoring of body image and state, and processing emotions. Also included in the list of possible resting activities is the ongoing internal “thought” processing that humans experience during resting consciousness, sometimes referred to as “stream of consciousness” (James, 1890). Since these “thought” processes are generally self-initiated and self-referential and not related to specific exogenous task demands, we use the term “task-unrelated thoughts” (TUTs) to describe them (Giambra, 1989, Shaw and Giambra, 1993, Singer, 1988). This term is comparable to others such as “stimulus independent thoughts” (SITs) (Antrobus, 1968, Teasdale et al., 1993, Teasdale et al., 1995) and “free association” (Andreasen and O'Leary, 1995).

Based on our previous findings and the work of others (Binder et al., 1999, Mazoyer et al., 2001, McKiernan et al., 2003, Shulman et al., 1997), we suggested a mechanism of reallocation of brain processing resources to account for some instances of TID (McKiernan et al., 2003). This model proposes that internally generated cognitive activities (such as TUTs) are suspended due to reduced availability of resources when attention shifts from ongoing, internal processes to performance of an exogenous task. In support of this hypothesis, we observed a correlation between task difficulty and the magnitude of TID in many brain regions (McKiernan et al., 2003). TID in these areas may thus stem from the attenuation of internally generated processes when attentional resources are required for performance of an effortful exogenous task. From this perspective, processing demands of the exogenous task should also influence the propensity for TUTs, in that more demanding exogenous tasks leave fewer resources available for “stream of consciousness” processing.

TUTs may be experienced as self-generated thoughts or daydreams, often with verbal or visual content (McGuire et al., 1996). The content of TUTs can include all of the “monitoring” activities listed above as well as problem solving, planning, and retrieval of memories. TUTs have biological significance in that these activities all serve to enhance the potential for survival and can make the individual more efficient and effective in managing their environment and their actions. Research indicates that thought processes of this nature are salient features of the resting state (Antrobus, 1968, Antrobus et al., 1966, Giambra, 1989, Giambra, 1995, Gusnard et al., 2001, James, 1890, McGuire et al., 1996, Pope and Singer, 1976, Posner and Rothbart, 1998, Singer, 1988, Teasdale et al., 1993, Teasdale et al., 1995). Self-reported thought content has been used as an indicator of the extent of internal processing activity (Antrobus, 1968, Antrobus et al., 1966, Giambra, 1989, McGuire et al., 1996, Pope and Singer, 1976, Shaw and Giambra, 1993, Singer, 1988, Teasdale et al., 1995). Early studies (Antrobus, 1968, Antrobus et al., 1966) described the effects of external task load on TUT frequency, noting that as more external information is presented, TUT frequency declines. Another study linked TUT frequency with processing resource availability by manipulating practice effects. Significantly more TUTs were reported when subjects had previously practiced motor or memory tasks than when practice was not completed (Teasdale et al., 1995). The theory of TID proposed above, as well as the results from these studies, suggests that TUT processing is interrupted by the presence of new information that requires priority processing. Thus, TUT processing is attention dependent and interruptible. It is also moderated by task difficulty, which determines the amount of processing resources required to be reallocated to the external task.

In a simulated scanning environment, we used a standardized query procedure to elicit thought content (TUT frequency) during the same auditory target detection task used in our previous experiment (McKiernan et al., 2003). As before, task difficulty was parametrically manipulated within each of three factors. These factors – stimulus presentation rate, target discriminability, and short-term memory load – were selected based on evidence that their manipulation influences task processing demands (Antrobus, 1968, Antrobus et al., 1966, Teasdale et al., 1993, Teasdale et al., 1995). We predicted a higher frequency of TUTs during rest than during any task condition. As task difficulty increased within each factor, we expected a decreased BOLD signal in TID regions and fewer TUTs. Additionally, TUT frequency was expected to correlate with the degree of TID, with the strongest correlations in brain regions associated with problem solving, planning, knowledge retrieval, and self-referential thought processing. Our goal is to link our previously established changes in TID in response to task difficulty manipulation with self-reported reductions in “stream of consciousness” processing.

Section snippets

Subjects

Thirty neurologically healthy subjects (19 women and 11 men), ranging in age from 18 to 49 years (M = 27.7, SD = 7.2), participated in the study. All were right-handed as defined by a laterality quotient >50 on the Edinburgh Handedness Inventory (Oldfield, 1971). fMRI data from 50% of the subjects in this study were included in our first study describing TID magnitude as a function of task difficulty (McKiernan et al., 2003); the fMRI data from the other 15 subjects are reported here for the

Results

Four subjects were removed from the analyses based on inspection of TUT session data: three as outliers because they did not indicate any TUTs during rest and one due to poor performance on the auditory target detection task. Behavioral data from both fMRI and TUT sessions (N = 26) are presented in Table 2. Paired t tests comparing task performance across sessions revealed no differences in performance except on accuracy in the most difficult discriminability condition, which was higher during

Discussion

As the auditory target detection task increased in difficulty (i.e., increased in processing demands), eight brain regions showed a correlated decline in fMRI BOLD signal (i.e., more negative TID values) relative to the resting state. Performance on the target detection task was equivalent during the fMRI and subsequent TUT session. TUT frequency also declined as the processing demands of the auditory task increased. In four of the eight brain regions of interest, decreases in fMRI BOLD signal

Conclusion

These results add to a growing understanding of the nature of task-induced deactivations commonly observed in functional neuroimaging studies. They suggest a link between the suspension of activity in specific brain regions and the attenuation of subjectively experienced thoughts, further supporting the suggestion that TID in these regions represents interruption of ongoing, cognitive processes present during resting states.

Acknowledgments

This research was supported by grants to JRB from the National Institute of Mental Health (PO MH51358) and National Institute of Neurological Disorders and Stroke (RO1 NS33576) and by the National Institutes of Health General Clinical Research Center (M01 RR00058) at MCW. We thank T. Prieto, T. Thelaner, B.D. Ward, and A. Moths for their technical assistance.

These data were presented in part at the 2001 Cognitive Neuroscience Society annual meeting.

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