Carl M. Anderson, Ph.D. Research Fellow, Mclean Hospital/Harvard Medical School
*Steven B. Lowen, Ph. D. Senior Research Associate, Electrical and Computer Engineering, Boston University
Perry Remshaw, M.D., Ph.D. Dir. Brain Imaging Center, Mclean Hospital/Harvard Medical School
Luis C. Maas, M.S., Research Fellow, MIT/Harvard Medical School
*Blaise Frederick, Ph.D. Assistant Biophysicist, Brain Imaging Center, Mclean Hospital/Harvard Medical School
*Lawrence L. Wald, Ph.D. Assistant Biophysicist, Massachusetts General Hospital NMR Center/ Instructor, Dept. of Radiology, Harvard Medical School.
Fredric Schiffer, M.D. Attending Psychiatrist, Mclean Hospital/Harvard Medical School.
Martin Teicher, M.D., Ph.D. Dir. Developmental Biopsychiatry Research Program, Mclean Hospital/Harvard Medical School
*new additions to the team (specific contrubutions are described in the proposal section).
Executive Summary
Overview:
We seek to explore the foundations of consciousness through the use of fMRI to examine the vertical convergence 6,10,88,91 of spontaneous fractal time 16,81,87 processes in the brain/mind/body. Specifically, the phenomena of mind wandering 13,148 will be investigated by observing coherence among fluctuations in physiological markers (heart rate, respiration, electrodermal activity [EDA]) and in fMRI signals from bilateral amygdaloid regions of the temporal lobes while subjects attempt meditation 12,37,76,101 or the recall of neutral or emotional memories 116. Fluctuations of thought, emotion or physiological markers appear to lack a characteristic time scale, and do not fit neatly into the "task A:task B" type of experimental design so prevalent in fMRI investigations of cognition 1.
Many of the non-periodic and irregular spontaneous processes of living systems have been observed to approximate fractals in time or space, i.e., lack a single absolute scale of measurement 107,149-151. Can the "stream" of consciousness be described as irregular or having "fractal" properties in time? Does spontaneous mind wandering lack a single scale of measurement in time? If this is indeed the case, then the methods of fractal mathematics (which allow quantification of structure or pattern across many spatial or temporal scales, resulting in a single measurement of multiscale order ) could be useful in the description of spontaneous fluctuations of the mind and body and how they vertically cohere 10,88,91 during different states of consciousness.
Spontaneous behavioral phenomena at all levels of organisms from ion channel currents 81,82 and neural spike trains 134-135 to REM sleep 9 and foraging patterns of animals 33,147 to reaction time fluctuations generated by subjects in cognitive science experiments 50 exhibit these recurrent fluctuations which were once tacitly overlooked and excluded as "noise" 10,11,16,149-152,156. The fractal nature of consciousness and its fluctuating "stream" of attention are consistent with the concept of vertical convergence 6,10,88,91, that the uniquely self-organizing 14,15 architecture of our bodies and our minds results from the coalescence of spontaneous self-similar fluctuations over many orders of space and time.
Activities:
-Investigate coherence among fractal fluctuations in both the left and right temporal lobes and physiological processes with state-of-the-art phased-array fMRI techniques during the mind wandering implicit in the task of meditation 76.
-Investigate the relation between emotions and spontaneous mind wandering by observing coherence among physiological fluctuations arising during the recall of neutral and negative emotional memories in the same subjects.
-Visualize the resulting fMRI dynamics on anatomical reconstructions of temporal lobe structures providing for the first time a 4-D view of cognitive processes which occur during meditation and emotional memory recall.
Results:
-We hypothesize that during both meditation and emotional memory tasks, extended bilateral spatio-temporal cortical-subcortical networks 28 centered on the amygdala 78 are activated and emerge over a wide range of time scales.
-We further hypothesize that the degree of interhemispheric coherence will covary with changes in physiological markers and different states of consciousness 2,6,24,27,29,30,41,62,72,77,80,89 92,97,101-104,112-123,125-127,129-133,136-138,140-146,153-155,158-159.
-Emergent coherent long-range-interactions among pixel intensity
fluctuations in the bilateral amygdala and fractal patterns of
physiological markers may underlie meditation and memory recall,
as well as delineate and visualize associated cognitive cortical
and subcortical networks.
Body of proposal
To what extent do brain, mind and body interact during the experience of consciousness? Also how do spontaneous fluctuations in thoughts, images, physical sensations and the sense of time occurring during meditation or under conditions of mild sensory deprivation (e.g.,Tank Isolation Technique 83) depend on this interaction? One of the great challenges facing the functional mapping of changes in brain physiology associated with different states of consciousness is to try and linearly isolate the elements of this interaction 1. The principle tenet underlying our approach to this challenge is that spontaneous changes in thought result from nonlinear interactions over a wide range of time scales among brain, mind and body. In particular, we will focus on the temporal lobe, where thought, feeling and emotion spontaneously converge, causing linear assumptions of time, space, cause and effect to break down during tasks such as watching one's own mind or remembering an experience.
1. Bridging Breath, Heart and Mind: The Bilateral Amygdala.
The amygdaloid complex 4,79, primarily a nexus of the basolateral amygdala (BLA) and extended amygdala (EA) 64 as well as other temporal and frontal lobe cortical and subcortical structures, may play a central role in focusing multisensory integration of emotionally relevant sensory information through multiple and largely reciprocal connections with the rest of the cortex, thalamus, and reticular formation (RF) 78. Unique to the BLA are "experiential phenomena" electrically evoked in humans during the course of stimulation to locate epileptic foci for surgical removal 51,52,61. Although these experiences embody the full range of emotions, fear and anxiety are the most common and are evoked frequently from the right amygdala. The following, from Gloor et al. 52, is a description of a childhood trauma memory evoked during electrical amygdaloid stimulation in an adult male prior to surgery:
"When the right amygdala was stimulated with a 1 mA current, {the patient} experienced something that he found difficult to describe but finally likened to a feeling of falling into water. {After another stimulation} [T]he patient immediately opened his mouth with an astonished look on his face, sat up, and said that now he knew what it was: it was the feeling of being at a picnic in Brewer Park in Ottawa. "A kid was coming up to me to push me into the water. It was a certain time, a special day during the summer holidays and the boy was going to push me into the water. I was pushed down by somebody stronger than me. I have experienced that same feeling when I had petit mals before. {...} When questioned whether he actually saw himself being threatened by the "big fellow" he said no, but it was a feeling as if he were there and was being chased."
How can one small brain region have so much control over our consciousness? It appears that normally the BLA-CNA-EA provides a kind of "binding" between cortical desynchronization control and brainstem autonomic feedback to emotionally significant sensory experience in order to, as Gloor states: "...attach affective tone...[to sensory experience]...to make a perception or memory emerge into consciousness, thus enabling it to be experienced as an event one is living or has lived through'." 52. On the basis of extensive anatomical and physiological evidence, Langhorst 78 postulated that the different regions of the amygdala such as the BLA and EA interact with the RF by various feedback loops to regulate heart rate and breathing, as well as desynchronization of the cortical EEG during arousal. The EA, for example, is coextensive with the basal forebrain regions which provide cholinergic drive to the cortex as well as monoaminergic cell body groups globally innervating the cortex from the RF 6,10,64,78,79. The central nucleus of the amygdala (CNA) is an important temporal lobe subcomponent of the EA and output funnel for the BLA 64,78,79,111. Schulz et al. 124 observed in chronically instrumented, awake cats that when discharge sequences recorded from single neurons in the CNA had slow rhythmical patterns of 5-12 s, blood pressure and EEG fluctuations were positively correlated. They proposed that the CNA is a key output structure of the amygdaloid complex and uses rhythmical patterns to coordinate somatomotor and vegetative systems in the RF during emotional experience. A commonly used marker of emotional states in humans is EDA 27,28,41. Although not strictly synchronized with respiration or arterial blood pressure waves, EDA fluctuations evoked by electrical stimulation of the amygdala in humans 97 also have oscillations well within the frequency range of respiration 106. Rittweger et al. 106, 107 observed that EDA-rhythms evoked in humans during different emotional states were related but not strictly synchronized with respiration or blood pressure waves. Thus, it appears that during many states of consciousness, long-range spatial and temporal correlations occur between forebrain structures such as the BLA, EA, thalamus, cortical and brainstem coherent with respiration, heart rate and autonomic changes, contributing to our affective experience of emotional states.
But again, how can this system have so much influence over our experience of consciousness? This question is explored at great length in LeDoux's The Emotional Brain 79. He concludes that the key is understanding how the amygdala interacts with working memory. Unfortunately, LeDoux presents a linear approach to describing the very nonlinear interactions between working memory and emotional experience. For example, he assumes that normally the amygdala is less functional during normal states of consciousness and only awakens to dangerous or negative emotional stimuli " ...then the amygdala is brought into the act and activates arousal systems (p. 290)". This linear, sequential point-of-view depicts the amygdala as only one specialized emotional element (although composed of immensely complex subsystems of elements 111) in a "quasi-deterministic" cognitive machine. In contrast to this linear perspective, we propose that the amygdala plays a dynamic role in creating what LeDoux calls "the here and now in the brain (p.272)." Pyramidal cells within the amygdala are in fact nodal points for vertical convergence among subcellular, cellular and network fluctuations 6,10,88,91 to enable, for example constant amygdaloid-brainstem feedback modulation of global bihemispheric monoaminergic systems, in addition to "broad-band-binding 10 " with temporal and frontal cortical areas. Fractal burst firing in these cells, a result of vertically convergent subcellular fluctuations, may, in the irregular cortex-like 64, loop-within-loop network of the BLA, function as access points in a fractal hyperspace of emotionally indexed memories 6, providing rapid feeling to-memory access, whether during everyday, moment-to-moment consciousness or seizure evoked experiential phenomena. We propose that, as dynamic nodes, the interplay between bilateral 144 amygdala-RF loops generates our " being here now" feeling-tone while we are on LeDoux's " Platform of Awareness (p. 278)." In short, fluctuations of flow in the "stream" of consciousness may have their origin in the complex multi-level interplay among the right and left amygdala, brain, mind and body.
2. Abnormal Asymmetry, Meditation, and Harmony Between the Left and the Right Amygdala
Abnormal hemispheric asymmetry, resulting from childhood abuse and involving alterations in the "cross talk" between bilateral amygdaloid regions, could result in poor cognitive integration and emotional regulation that chartacterize a wide range of psychiatric disorders from depression to dissocated states 6, 74, 90. Previous work from our group has demonstrated the profound and persistent neural and psychological changes induced by early trauma in EEG evidence of asymmetric hemispheric activation during the recall of past trauma 7,114-120,136,137. Schiffer, Teicher and Papanicolau 116, using probe evoked potentials, found that recall of a traumatic childhood memory shifted cortical activity from left-sided predominance to right-sided predominance, and that the degree of right shift correlated with the severity of early childhood abuse.
A large body of research indicates that the right hemisphere may be specialized for processing negative emotions 2,5,7,34-37,40-43,109,112-123,129-131,142,143,145,153-155,158,159. Galin 47 and Joseph 72 speculated that painful childhood memories may be preferentially stored in the right hemisphere, outside of consciousness, but capable of influencing conscious behavior and affect. The work of Ito 69 suggests that childhood abuse may be associated with greater left-sided dysfunction, which may lead to greater dependence on the right amygdala. Increased dependence on the right amygdala may, in turn, lead to enhanced perception of and reaction to negative affect 47 and facilitate unconscious storage of painful childhood memories 72. Such speculation is consistent with clinical observations that traumatized individuals are often hypersensitive to the perception of negative affect, and that memories of early abuse may be fully repressed, but eventually retrievable 114.
As part of our ongoing study of early abuse on brain development, Schiffer et al. 119 found that left or right visual stimulation altered the affect and theta EEG laterality of college students. On a separate day each student underwent an echo planar fMRI scan using a unique T2 stepping procedure to assess T2 relaxation time as an indirect non-invasive estimate of basal blood perfusion in each hemisphere and in anterior temporal lobe (ATL). Right-sided resting ATL blood flow determined by baseline fMRI appeared to predict EEG and affect responses to lateral visual field stimulation 120. This was further supported by our findings that in normal students fMRI analysis indicated an extremely tight coupling between right and left hemisphere T2 measurements (r = 0.995) with a slope that is extremely close to unity (b=1.048). In contrast, (see Figure 1) abused subjects had a lower correlation (r=0.861).
Taken together with the ground breaking work of Sperry 132 and others 115, these findings support a unique view 6, 74 that in terms of emotional cognition our two hemispheres are like dual joined minds, or mental Siamese twins, harmoniously sharing and integrating emotional experience. This cognitive-emotional integration is disrupted by early abuse or traumatic events which can unbalance these twins and lead to pathological struggles for emotional dominance resulting in a wide range of personality disorders. For example, one twin, the right in many cases, may retain the memory of abuse or trauma, and, as a result, be functionally less mature. In times of stress or anger, it may take control, sabotaging the good efforts of the more mature personality resulting in acts of violence, child abuse, self-destructive behavior or the appearance of alters. These perpetual interhemispheric struggles, primarily a result of child abuse, may be the psychological root of drug addiction and personality disorders 6.
abused subjects had a lower correlation (r=0.861).
Taken together with the ground breaking work of Sperry 132 and others 115, these findings support a unique view 6, 74 that in terms of emotional cognition our two hemispheres are like dual joined minds, or mental Siamese twins, harmoniously sharing and integrating emotional experience. This cognitive-emotional integration is disrupted by early abuse or traumatic events which can unbalance these twins and lead to pathological struggles for emotional dominance resulting in a wide range of personality disorders. For example, one twin, the right in many cases, may retain the memory of abuse or trauma, and, as a result, be functionally less mature. In times of stress or anger, it may take control, sabotaging the good efforts of the more mature personality resulting in acts of violence, child abuse, self-destructive behavior or the appearance of alters. These perpetual interhemispheric struggles, primarily a result of child abuse, may be the psychological root of drug addiction and personality disorders 6.
Figure 1. Relationship between left and right hemisphere values of T2 relaxation time based on fMRI using T2 stepping. Each point represents an individual subject. Data for normal controls (dot) falls along expected regression line for identical right/left measures. Abused subjects (square) fall along a different line with more shallow slope and higher left hemisphere y-intercept. and flatter slope, indicating an excess of right hemispheric activity (6). We also hypothesize that this binding may occur over a multitude of time scales during recall (this is why it takes time to re-experience these memories).
3. The Fractal Geometry of Time in Neurobiology and Consciouness.
It is frequently assumed that many biological and natural processes are best described as random independent sequences, and many are still widely perceived, studied and modeled under this assumption. Bohm and Peat 22 commented on how a breakdown in communication in scientific work can result from different and incompatible ways in which the informal language of science is used. Take, for example, the word random: random numbers from a computer generator appear to lack any degree of order, when in fact the numbers are produced in a very ordered and deterministic fashion. Randomness is relative and context dependent. The definition of randomness as lacking all order "has no real meaning...[because]....random events do happen to take place in a definable and describable sequence and can be distinguished from other random events....in this elementary sense they obviously have an order ( p. 128). 22 "
A revolution in the scientific perception of many noisy natural processes began with Benoit Mandelbrot's 1983 book 87The Fractal Geometry of Nature. Fractal geometry has evoked a fundamentally new view of how living and nonliving matter is organized into complex recursively nested patterns over multiple levels of space or time. Patterns termed "fractal" or "self-similar" are recurrently irregular in space or time, with themes repeated like the layers of an onion at different levels or scales.
The term fractal applies to objects in space or fluctuations in time that possess a form of self-similarity: fragments of the object or sequence can be made to match the whole object or sequence by shifting and stretching. Fragments of fractal objects can be exact or statistical copies of the whole. Mathematical fractal objects visually convey the concept of self-similarity. However, only fragments of mathematical fractal objects can be exact copies, and exactly represent the concept of self-similarity, whereas the fragments of natural fractals are only statistically related to the whole. Another way to think of fractals is in terms of clusters of points or events in space or time. Self-similar clusters have smaller clusters within larger clusters of clusters. Clouds, broccoli, or the surface of the brain can all be visualized as clusters of clusters in space. Temporal fractal scaling relationships have now been observed in many physiological processes that have relevance to fMRI measurements, such as blood flow 16, 110 ,
cardiology 11,55,56,75,139 and respiration activity 68. In fact, there is a growing consensus by a number of groups 8,19-21,71,85,100,152 that physiological fluctuations constitute an important source of "noise" in fMRI images. Many physiological processes (e.g., respiration, pulsatile flow, vasomotor oscillations and other low frequency fluctuations) could contribute through any number of ways to the noise observed in fMRI images 20,152.
An alternative perspective taken in this application is that noise in fMRI images may in fact constitute a complex non-periodic signal that has its origins in the fractal fluctuations of the underlying neurobiological processes associated with consciouness. Therefore, we propose that physiological processes which are integral to the experience and measurement of different states of consciousness may provide an external signal to correlate with internal self-organizing cortical-subcortical networks.
Figure 2. Temporal lobe regions imaged with a phased array detector and special head coils (FSE oblique, 3.0mm thick interleaved TR/TE = 4s/124ms, ETL = 16, 24x18cm FOV, 512x384 matrix, 3Nex, 8:05 imaging time).
4. Experimental Methods
4.1 Scanning To a significant extent, physiological processes produce time-dependent fluctuations in the fMRI BOLD signal during tasks. To ascertain the magnitude of the contribution and correlation with brain activation, EKG, respiratory and EDA recordings will be taken concurrently with the long time series of echo planar BOLD fMRI images (6 planes of 1200 interleaved images collected at a repetition time [TR] of 1 s) from normal adults. Movement artifacts will be removed using the DART image registration package 86. After motion correction time series will be further processed by Dr. Lowen. All imaging will be performed on a 1.5-T GE Signa system equipped with a whole-body echo planar gradient set (Advanced NMR Systems) and special head coils (We have also developed state of the art phased array detectors and coils to enhance visualization of the bilateral temporal lobes [see Wald & Frederick CV's; and Figure 2] during anatomical MRI and BOLD fMRI). Baseline fluctuations in the fMRI signal will be examined in 10 subjects, (5 male; 5 female) who will be instructed to remain motionless (except when signling mindwandering (see task]) , with their eyes closed during three 20 minute acquisition periods with interposed 10 min rest period. Two sets of 1200 echo-planar images will be collected (gradient echo, TE=40ms, TR=1s, flip angle=66°, thickness=5mm; in-plane resolution=3.125 x 3.125 mm) in six axial planes from mid-body of the amygdaloid complex toward the caudate. A standard set of phased array anatomical images will also be collected. ECG will be measured with standard Omni-Track (3100) MRI ECG Cable (Invivo Research Inc.,Orlando Fl) and 0.75 inch diameter (or greater) electrodes. Respiration will be monitored by use of the Omni-Track noninvasive electrical impedance plethmography off the EKG electrodes. EDA will be recorded with a non-metalic electrode that is adhered to the right hand, with signals sent to the A/D by way of a standard MRI ECG cable. All physiological recordings will be acquired through the LAB-VIEW software system at 50Hz. All subject EKG preparation will be performed by qualified personnel at the McLean MRI center.
4.2 Task Right handed young adults between 18-22 years of age, unmedicated, and not using illicit substances, will be recruited by poster and web site.
The meditation period of the experiment will occur during the first 20 min scan. After entering the scanner the subject will be asked to close his or her eyes, focusing attention and maintaining it on the physical sensation of air entering the nasal passages. In addition, the subject will be instructed to push a button to indicate when they realize their mind has wandered from the breath meditation. The subjects will not be told that the task involves meditation. Emotional and neutral memories will be reviewed with a psychodynamic therapist prior to entering the scanner ( based on the task described in Schiffer et al. 116 ).
During the 2nd 20 min scan the subject will be asked to remember and reflect on a recent ordinary work or school situation. Again, the subject will be instructed to push a button to indicate when they realize their mind has wandered from the task. Emotional state will be assessed verbally by asking the subject to rate his or her present feelings for each of eight affects from an abbreviated POMS scale, from none to extreme on a 5 point scale. The eight affects measured will be: anxiety, tension, anger, sadness, hopelessness, panic, nervousness, and guilt.
After a 5 to 10 min rest period the subject will then be asked to affectively reexperience an emotion memory or experience as reviewed with a psychodynamic therapist prior to entering the scanner. Again, the subject will be instructed to push a button to indicate when they realize their mind has wandered from the task. The procedure would be discontinued if the subjects requests or seems unduly upset. The subject will then be assessed again with the abbreviated POMS scale. The unpleasant memory task will always be presented after the neural memory task because of the concern that lingering effects of the unpleasant memories would interfere with the neutral task. After completion of the scan, a psychodynamic therapist will work with each subject to restore the subject's usual mood if required.
4.3. Analysis: T1 weighted images will be acquired both for clinical review and for computer assisted morphometry using MEDx (medxsales@sensor.com). MEDx will also be used to align subject data sets collected over single or multiple sessions. For all images, brain landmarks will be identified and subsequently normalized to the Talairach atlas system with distances scaled proportionately to these landmarks (Surface and AIR 3.0 will be used in addition to Talairach Transformations). Possible anatomical changes, such as varations in gray/white matter ratios, CC and other commisural systems will also be investigated during anatomical analysis and image segmentation. 3D surface and volume rendering as well as volume reformatting and regional analysis will be used extensively in visualizing and animating the results of Dr. Lowen's functional analysis algorithms on the PI's SGI work station.
5. Hurst Analysis of Physiological Fluctuations in Functional MRI
In the absence of stimuli, functional MRI (fMRI) data may contain a wealth of information related to dynamic interactions, i.e. functional connectivity, among multiple brain regions. Traditional signal processing techniques, however, extract only limited information over a single time scale. Thus, we examined one multiscale method, Hurst's Rescaled Range Analysis, as a potential tool to identify brain regions with similar fMRI signal patterns over multiple time scales. All imaging was performed on a 1.5-T GE Signa system (as described above) in two axial planes through the caudate. Images were corrected for frame-to-frame motion with the DART registration algorithm. The time series were subjected to Hurst's Rescaled Range Analysis , a technique which examines correlation within the data set over multiple time scales. In this method, the range R of the cumulative deviation of signal intensities is normalized by the standard deviation S in data windows of increasing length N. For each pixel, the power law exponent H is measured as the slope of log(R/S) vs. log(N). H can be intuitively understood as a probability directional change-how increases in the sequence are likely to be followed by increases and decreases by decreases over various time scales. H = 0.5 indicates an uncorrelated sequence of signal intensity values; H > 0.5 is called "persistence" since changes are in the same direction; H < 0.5 suggests that the directions of change over time will be successively opposite. Although H was computed on a pixel-wise basis, brain regions with similar values of H exhibit fluctuations with similar temporal scaling structures, and thus may be related functionally.
Local clustering of persistent H values (H > .5) was observed bilaterally in the frontal cortical regions in both slices (Fig 3 A&B). As expected, H values near 0.5 dominate the regions outside the head.
B.
Figure 3. (A) Top and (B) bottom slice.
In this preliminary analysis of fMRI data with the Hurst exponent H, we identified regions with similar patterns of fluctuations over multiple time scales. Although the meaning of H in this context is not yet known, this fractal characteristic may provide insight into functional relationships. Whether the clusters of persistent H values originate primarily from neuronal or other physiological processes (e.g. respiration, pulsatile flow, vasomotor oscillations) (4) or a combination remains to be investigated.
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