Elsevier

NeuroImage

Volume 45, Issue 4, 1 May 2009, Pages 1047-1054
NeuroImage

Comments and Controversies
Neurophysiology of functional imaging

https://doi.org/10.1016/j.neuroimage.2008.08.026Get rights and content

Abstract

The successes of PET and fMRI in non-invasively localizing sensory functions had encouraged efforts to transform the subjective concepts of cognitive psychology into objective physical measures. The assumption was that mental functions could be decomposed into non-overlapping, context-independent modules that are operated on by separable areas of a computer-like brain. The failures of cognitive modularity and of a very localized phrenology are generally, but not universally, accepted; but in their place, and usually not distinguished from the original revolutionary hopes of clarification, experimental results are being interpreted in terms of rather flexible definitions of both cognitive concepts and the degree of localization. In an alternative approach, we have connected fMRI, 13C MRS, and electrophysiology measurements of brain energy to connect with observable properties of mental life (i.e., awareness). We illustrate this approach with a sensory stimulation experiment; the degree of localization found in BOLD signals was related to the global energy of the brain which, when manipulated by anesthetics, affected the degree of awareness. The influence of brain energy upon functional imaging maps is changing the interpretations of neuroimaging experiments, from psychological concepts generating computer-like responses to empirical responses dominated by the high brain energy and signaling at rest. In our view “baseline” is an operational term, an adjective that defines a property of a state of the system before it is perturbed by a stimulus. Given the dependence of observable psychological properties upon the “baseline” energy, we believe that it is unnecessarily limiting to define a particular state as the baseline.

Introduction

Non-invasive brain imaging methods (i.e., PET and fMRI) have had tremendous success in localizing sensory functions. Using the simple differencing method, primary motor and sensory cortices can be reliably mapped with results matching those previously only found by invasive methods (Hubel and Wiesel, 1959, Wandell et al., 2007). For more complex mental functions, such as language, fMRI can show hemispheric dominance so reliably that it is now used to guide surgical decisions in patients with refractory epilepsy (Medina et al., 2007). These successes have encouraged scientists to use neuroimaging to address psychological questions in an effort to transform the contingent, subjective concepts of psychology and everyday life into communicable understandings with the objectivity of physical science.

Section snippets

Cognitive neuroimaging

In the earliest years of functional imaging, its main focus was on Neurophysiology so as to determine the regulation of cerebral metabolism and blood flow during brain function. The first SPECT and PET maps of brain activity in response to cognitive concepts were so beautiful that they raised hopes for exploring psychology (Lassen et al., 1978, Reivich et al., 1983). As PET and fMRI developed the ability to map responses to mental stimuli, the techniques became more widely used for experiments

The modularity concept

The philosophical problem of defining concepts of mental function was a primary concern of Ludwig Wittgenstein, who showed that only mathematical or logical terms can be unequivocally defined, whereas even simple terms like “chair” defy explanations that would identify all objects we regard as chairs and exclude all that we do not (Wittgenstein, 1953). Once we recognize that common objects cannot be defined with the rigor of logic, we realize how revolutionary it would be if words like “working

Delocalized activity

The difficulties besetting the modularity concept were seen in a wide range of fMRI experiments. It has become apparent that cortical activations in response to cognitive activity were widespread, being found in many regions, instead of being reproducibly localized as were the primary responses to sensory inputs. This dealt a blow to the hope that even though cognitive concepts might not strictly be defined by modules of brain functions; still brain localization would make concepts more

Negative BOLD

Cognitive Neuroscience in addition to assuming psychological modules had also postulated that the modules were operated on by a computer-like brain although the details of such processing had no consensus. The assumption of a computer-like brain was confounded by results showing that imaging signals observed in certain brain regions were rather consistently negative during stimulation (Shulman et al., 1997). By the time that negative BOLD signals became noteworthy, the role of cerebral

fMRI and energy based neuroscience

The combination of fMRI, 13C MRS, and electrophysiology has allowed the energy consumption of the many neurons in an fMRI voxel to be correlated with the electrical activity of ensembles of individual neurons in the same volume. Results from electrophysiological, fMRI, and 13C MRS experiments are expressed in terms of the fundamental physical parameter of energy consumption: the cerebral metabolic rate of oxygen consumption (CMRO2) since essentially all brain energy comes from the oxidation of

Effects of baseline energy on fMRI

To explore the neuronal foundations of baseline and incremental energetics, we conducted electrophysiological and fMRI studies in rats at two anesthetic states, characterized by very different baseline energies (Maandag et al., 2007); the lower energy state (α-chloralose) was 40–60% lesser than the higher energy state (halothane). Forepaw stimulation was administered in both states to excite the contralateral primary somatosensory cortex (S1). There were major differences between the two states

Empirical studies of brain function

The dynamic interplay between experimental results and scientific hypotheses described above reflects the excitement of science, the movement from one issue to the next that is raised in the course of study. In contrast to the assumptions of Cognitive Psychology that there were concepts of Mind in need of definition, we propose that mental activity can be studied by the reliable techniques of contemporary neurophysiology, certainly including fMRI and PET, without making revolutionary a priori

Shifting paradigm of psychological studies

The physiological studies of cerebral energetics combined with fMRI are profoundly changing the psychological interpretation of Cognitive Neuroimaging. Prominent early proponents of Cognitive Neuroscience, facing the growing experimental failings of modularity and cerebral localization, have been developing alternate descriptions of brain function that utilize neurophysiological results (Raichle and Mintun, 2006). In the past five years it would not be an exaggeration to say that the

Acknowledgments

This work was supported by NIH grants (R01 MH-067528, R01 DC-003710, R01 NS-037527, R01 NS-051854, P30 NS-52519). We thank Dr. Jennifer K. Roth for comments on the manuscript.

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