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PubMed1995

Towards measurement of brain function in operational environments.

In operational environments that demand sustained vigilance or that involve multiple tasks competing for limited attentional resources, continuous monitoring of the mental state of the operator could decrease the potential for serious errors and provide valuable information concerning the ergonomics of the tasks being performed. There is widespread discussion and appreciation of the basic feasibility of utilizing neurophysiological measurements to derive accurate, reliable, rapid and unobtrusive assessments of mental state. However, progress in transitioning this idea into practical applications has been impeded by the fact that at present no convenient, inexpensive and effective means exists to derive a meaningful index of brain activity outside of laboratory settings. In this paper, we review some recent advances in recording technology and signal processing methods that will help overcome this limitation. For example, rapid progress is being made in the engineering of recording systems that are small, rugged, portable and easy-to-use, and thus suitable for deployment in operational environments. Progress is also being made in the development of signal processing algorithms for detecting and correcting recording artifacts and for increasing the amount of useful information that can be derived from brain signals. Finally, results from basic research studies suggest that accurate and reliable inferences about the mental load and alertness of an individual can be derived from neurophysiological measures in a practical fashion. These research and engineering successes suggest that it is reasonable to expect that in the near term a basic enabling technology will be deployed that will permit routine measurement of brain function in operational environments.

Arousal↗

PubMed2002

Comparison of functional brain PET images and intraoperative brain-mapping data using image-guided surgery.

OBJECTIVE: Knowledge about the spatial localization of eloquent brain areas is essential for resecting lesions in the vicinity of these areas. The classical approach is to perform surgery on the awake patient under local anesthesia using brain-mapping techniques. As an alternative, the location of eloquent areas can be visualized by preoperative functional brain-imaging techniques, for example, positron emission tomography (PET), functional magnetic resonance imaging (fMRI), or magnetoencephalography (MEG). Using functional activation PET, both methods were combined by integration into a frameless navigation system (BrainLAB) and used to map speech-eloquent areas. PATIENTS AND METHODS: Speech-eloquent areas were localized preoperatively in seven patients with a left-sided glioma using 2-[(18)F]-2-desoxy-D-glucose PET. Patients were scanned under silence conditions (i.e., with the patient remaining silent in a sound-proof cabin), and speech was activated using a verb-generation paradigm. The PET data were transferred to the neuronavigation workstation and matched with a preoperative 3D-MRI using an automatic image-fusion algorithm. Intraoperative speech localization was performed using brain-mapping techniques under local anesthesia with bipolar cortical stimulation. The stimulator position was mapped into the MRI/PET data set by neuronavigational tracking of the instrument. RESULTS: Functional PET images were integrated into the MRI-based neuronavigational system and could be transferred exactly to the operative field. By the additional integration of cortical stimulation, intraoperative electrophysiological findings can be directly compared with preoperative functional images. Seven patients with left-sided glioma were operated on using this protocol, confirming the technical feasibility. In three of seven patients, preoperative PET findings were not supported by intraoperative mapping. CONCLUSIONS: This matching and mapping technique is suitable for monitoring eloquent speech areas during surgical resection of extensive left-sided low-grade gliomas, allowing a direct comparison between intraoperative electrophysiological brain mapping and preoperative functional brain-imaging findings. The sensitivity and specificity of functional imaging techniques can now be evaluated by reconciling the data with the intraoperative stimulation results.

Adult↗

PubMed2001

Signaling and gene expression in the neuron-glia unit during brain function and dysfunction: Holger Hydén in memoriam.

Holger Hydén demonstrated almost 40 years ago that learning changes the base composition of nuclear RNA, i.e. induces an alteration in gene expression. An equally revolutionary observation at that time was that a base change occurred in both neurons and glia. From these findings, Holger Hydén concluded that establishment of memory is correlated with protein synthesis, and he demonstrated de novo synthesis of several high-molecular protein species after learning. Moreover, the protein, S-100, which is mainly found in glial cells, was increased during learning, and antibodies towards this protein inhibited memory consolidation. S-100 belongs to a family of Ca(2+)-binding proteins, and Holger Hydén at an early point realized the huge importance of Ca(2+) in brain function. He established that glial cells show more marked and earlier changes in RNA composition in Parkinson's disease than neurons. Holger Hydén also had the vision and courage to suggest that "mental diseases could as well be thought to depend upon a disturbance of processes in glia cells as in the nerve cells", and he showed that antidepressant drugs cause profound changes in glial RNA. The importance of Holger Hydén's findings and visions can only now be fully appreciated. His visionary concepts of the involvement of glia in neurological and mental illness, of learning being associated with changes in gene expression, and of the functional importance of Ca(2+)-binding proteins and Ca(2+) are presently being confirmed and expanded by others. This review briefly summarizes highlights of Holger Hydén's work in these areas, followed by a discussion of recent research, confirming his findings and expanding his visions. This includes strong evidence that glial dysfunction is involved in the development of Parkinson's disease, that drugs effective in mood disorders alter gene expression and exert profound effects on astrocytes, and that neuronal-astrocytic interactions in glutamate signaling, NO synthesis, Ca(2+) signaling, beta-adrenergic activity, second messenger production, protein kinase activities, and transcription factor phosphorylation control the highly programmed events that carry the memory trace through the initial, signal-mediated short-term and intermediate memory stages to protein synthesis-dependent long-term memory.

Animals↗

PubMed1992

Deterministic nonlinear chaos in brain function and borderline psychopathological phenomena.

There exists a fundamental overall property of the brain which monitors, modulates, and ensures a smoothness of function and which further determines elegance and grace in functioning. This property also imparts a quality of, or a sense of proportion among all other faculties of the brain. It is postulated in this paper that such a property/function, up to now almost taken for granted, is maintained/exercised by a nonlinear deterministic chaotic mode of brain function. If this is the case, borderline psychopathological phenomena, when they flare up, can be explained as resulting from sudden reduction of such a deterministic chaotic mode and the emergence of a pathological order, as the system becomes an oscillating one.

Borderline Personality Disorder↗

PubMed2002

In vivo neuroanatomy of Alzheimer's disease: evidence from structural and functional brain imaging.

In vivo structural (CT, MRI) and functional (SPECT, PET) brain imaging techniques have been widely used to study the neuroanatomy and neurophysiology of Alzheimer's disease (AD) and to identify definite biological markers of the disease. We used meta-analytic methods to synthesize this literature to determine what neuroanatomical structures best differentiate patients with AD from healthy normal controls. A total of 125 studies published between 1984 and 2000 that included 3543 patients with AD and 1698 normal healthy controls met inclusion criteria. We found that measures of the temporal cortices, including the amygdala, hippocampus, and inferior temporal lobes, along with the anterior cingulate cortex, associated with the largest magnitudes of effects and, hence, could serve as the most useful structures to help clinicians differentiate AD from healthy normal aging.

Aged↗

PubMed2004

Activity in ventromedial prefrontal cortex covaries with sympathetic skin conductance level: a physiological account of a "default mode" of brain function.

We examined neural activity related to modulation of skin conductance level (SCL), an index of sympathetic tone, using functional magnetic resonance imaging (fMRI) while subjects performed biofeedback arousal and relaxation tasks. Neural activity within the ventromedial prefrontal cortex (VMPFC) and the orbitofrontal cortex (OFC) covaried with skin conductance level (SCL), irrespective of task. Activity within striate and extrastriate cortices, anterior cingulate and insular cortices, thalamus, hypothalamus and lateral regions of prefrontal cortex reflected the rate of change in electrodermal activity, highlighting areas supporting transient skin conductance responses (SCRs). Successful performance of either biofeedback task (where SCL changed in the intended direction) was associated with enhanced activity in mid-OFC. The findings point to a dissociation between neural systems controlling basal sympathetic tone (SCL) and transient skin conductance responses (SCRs). The level of activity in VMPFC has been related to a default mode of brain function and our findings provide a physiological account of this state, indicating that activity within VMPFC and OFC reflects a dynamic between exteroceptive and interoceptive deployment of attention.

Adult↗

PubMed1989

Hypothermia protects brain function in acute carbon monoxide poisoning.

The role of body temperature in the morbidity and mortality resulting from acute severe carbon monoxide (CO) poisoning (2400 ppm CO, 90 min) was investigated using an unanesthetized animal model. Modified Levine prepared female rats (left common carotid artery and jugular cannulated) displayed a lower rate of recovery period (4 hr) re-warming, and an increased mortality rate and behaviorally-assessed neurologic index (NI) compared to normal rats. This indicated their greater susceptibility to CO hypoxia, although the degree of CO-induced hypothermia was the same in both groups. The whole-body cooling of Levine rats to a similar extent prior to CO exposure increased somewhat the post-CO re-warming rate, and marginally decreased NI and mortality during CO exposure (in-CO). In contrast, maintenance of constant body temperature by external heating during CO exposure resulted in a negative post-CO re-warming rate and sharply increased NI and in-CO mortality. Normal euthermic rats were much less severely affected by CO. The results suggest that hypothermia, whether CO-induced or produced by prior cooling, provides measurable protection of brain function during acute severe CO poisoning, and that maintenance of body temperature increases in-CO mortality and interferes with ability to thermoregulate and increases NI in survivors.

Animals↗

PubMed2006

Simplified ultrasound screening for fetal brain function based on behavioral pattern.

Despite the longstanding conclusion that behavior can reveal aspects of underlying anatomy and function, no generalized antenatal behavior screening has been developed to identify fetuses that may have central nervous system defects requiring further evaluation. We devised a brief ultrasound examination to distinguish fetuses with compromised central nervous system function from the general population and evaluated it with this study. The study design compared behavioral findings obtained by retrospectively reviewing the ultrasound examinations of 5 fetuses that had abnormal behavior with prospectively obtained findings of 29 normal fetuses. Median time for brief examination criteria was 50 min (range, 30-60 min). The only case undetectable by this brief ultrasound examination has an eye-movement period significantly longer than the normal upper limit. Using this method as a screening test may make it possible to include assessment of fetal brain function as part of routine antenatal care.

Central Nervous System↗

PubMed2001

Genetics of brain function and cognition.

There is overwhelming evidence for the existence of substantial genetic influences on individual differences in general and specific cognitive abilities, especially in adults. The actual localization and identification of genes underlying variation in cognitive abilities and intelligence has only just started, however. Successes are currently limited to neurological mutations with rather severe cognitive effects. The current approaches to trace genes responsible for variation in the normal ranges of cognitive ability consist of large scale linkage and association studies. These are hampered by the usual problems of low statistical power to detect quantitative trait loci (QTLs) of small effect. One strategy to boost the power of genomic searches is to employ endophenotypes of cognition derived from the booming field of cognitive neuroscience. This special issue of Behavior Genetics reports on one of the first genome-wide association studies for general IQ. A second paper summarizes candidate genes for cognition, based on animal studies. A series of papers then introduces two additional levels of analysis in the "black box" between genes and cognitive ability: (1) behavioral measures of information-processing speed (inspection time, reaction time, rapid naming) and working memory capacity (performance on on single or dual tasks of verbal and spatio-visual working memory), and (2) electrophyiosological derived measures of brain function (e.g., event-related potentials). The obvious way to assess the reliability and validity of these endophenotypes and their usefulness in the search for cognitive ability genes is through the examination of their genetic architecture in twin family studies. Papers in this special issue show that much of the association between intelligence and speed-of-information processing/brain function is due to a common gene or set of genes, and thereby demonstrate the usefulness of considering these measures in gene-hunting studies for IQ.

Brain↗

PubMed2005

Resolution, sensitivity and precision with autoradiography and small animal positron emission tomography: implications for functional brain imaging in animal research.

Quantitative autoradiographic methods for in vivo measurement of regional rates of cerebral blood flow, glucose metabolism, and protein synthesis contribute significantly to our understanding of phsysiological and biochemical responses of the brain to changes in the environment. A disadvantage of these autoradiographic methods is that experimental animals can be studied only once. With the advent of small animal positron emission tomography (PET) and with increases in the sensitivity and spatial resolution of scanners it is now possible to use adaptations of these methods in experimental animals with PET. These developments allow repeated studies of the same animal, including studies of the same animal under different conditions, and longitudinal studies. In this review we summarize the tradeoffs between the use of autoradiography and small animal PET for functional brain imaging studies in animal research.

Animals↗

PubMed2005

Applications of GRID in clinical neurophysiology and Electrical Impedance Tomography of brain function.

The computational requirements in Neurophysiology are increasing with the development of new analysis methods. The resources the GRID has to offer are ideally suited for this complex processing. A practical implementation of the GRID, Condor, has been assessed using a local cluster of 920 PCs. The reduction in processing time was assessed in spike recognition of the Electroencephalogram (EEG) in epilepsy using wavelets and the computationally demanding task of non-linear image reconstruction with Electrical Impedance Tomography (EIT). Processing times were decreased by 25 and 40 times respectively. This represents a substantial improvement in processing time, but is still sub optimal due to factors such as shared access to resources and lack of checkpoints so that interrupted jobs had to be restarted. Future work will be to use these methods in non-linear EIT image reconstruction of brain function and methods for automated EEG analysis, if possible with further optimized GRID middleware.

Computer Systems↗

PubMed1989

Noninvasive functional brain mapping by change-distribution analysis of averaged PET images of H215O tissue activity.

Change-distribution analysis and intersubject averaging of subtracted positron emission tomography (PET) images are new techniques for detecting, localizing, and quantifying state-dependent focal transients in neuronal activity. We previously described their application to cerebral blood flow images (intravenous bolus H215O, Kety autoradiographic model). We now describe their application to images of H215O regional tissue activity without conversion to units of blood flow. The sensitivity and specificity of response detection and the accuracy of response localization were virtually identical for the two types of images. Response magnitude expressed in percent change from rest was slightly, but consistently smaller in tissue-activity images. Response magnitude expressed in z-score was the same for the two-image types. Most research and clinical applications of functional brain mapping can employ images of H215O tissue activity (intravenous bolus, 40-sec nondynamic scan) without conversion to units of blood flow. This eliminates arterial blood sampling, thereby simplifying and minimizing the invasivity of the PET procedure.

Adult↗

PubMed1995

Functional brain imaging with SPECT in normal aging and dementia. Methodological, pathophysiological, and diagnostic aspects.

New developments in instrumentation, radiochemistry, and data analysis, particularly the introduction of 99M TC-labeled brain-retained tracers for perfusion studies, have opened up a new era of single photon emission computed tomography (SPECT). In this review critical methodological issues relating to the SPECT instrument, the radioactive tracers, the scanning procedure, the data analysis and interpretation of data, and subject selection are discussed together with the changes in regional cerebral blood flow (rCBF) observed in normal aging. An overview is given of the topography and the pathophysiological and diagnostic significance of focal rCBF deficits in Alzheimer's disease and in other dementia disorders, in which SPECT is capable of early or preclinical disease detection. In Alzheimer's disease, the diagnostic sensitivity and specificity of focal rCBF deficits measured with SPECT and brain-retained tracers are very high, in particular when combined with medial temporal lobe atrophy on CT. Together with neuropsychological testing, SPECT serves to map the topography of brain dysfunction. Thus, in the clinical setting, SPECT provides information that is supplemental to that obtained in other studies. Future applications include neuroreceptor studies and treatment studies, in which SPECT may serve as a diagnostic aid in the selection of patients and as a potential mean for monitoring treatment effects. Although positron emission tomography is the best characterized tool for addressing some of these clinical and research issues in dementia, only the less expensive and technically simpler SPECT technique will have the potential of being available as a screening diagnostic instrument in the clinical setting. It is concluded that, properly approached, functional brain imaging with SPECT represents an important tool in the diagnosis, management, and research of dementia disorders.

Aging↗

PubMed2004

Human auditory evoked potentials in the assessment of brain function during major cardiovascular surgery.

Focal neurologic and intellectual deficits or memory problems are relatively frequent after cardiac surgery. These complications have been associated with cerebral hypoperfusion, embolization, and inflammation that occur during or after surgery. Auditory evoked potentials, a neurophysiologic technique that evaluates the function of neural structures from the auditory nerve to the cortex, provide useful information about the functional status of the brain during major cardiovascular procedures. Skepticism regarding the presence of artifacts or difficulty in their interpretation has outweighed considerations of its potential utility and noninvasiveness. This paper reviews the evidence of their potential applications in several aspects of the management of cardiac surgery patients. The sensitivity of auditory evoked potentials to the effects of changes in brain temperature makes them useful for monitoring cerebral hypothermia and rewarming during cardiopulmonary bypass. The close relationship between evoked potential waveforms and specific anatomic structures facilitates the assessment of the functional integrity of the central nervous system in cardiac surgery patients. This feature may also be relevant in the management of critical patients under sedation and coma or in the evaluation of their prognosis during critical care. Their objectivity, reproducibility, and relative insensitivity to learning effects make auditory evoked potentials attractive for the cognitive assessment of cardiac surgery patients. From a clinical perspective, auditory evoked potentials represent an additional window for the study of underlying cerebral processes in healthy and diseased patients. From a research standpoint, this technology offers opportunities for a better understanding of the particular cerebral deficits associated with patients who are undergoing major cardiovascular procedures.

Body Temperature↗

PubMed2004

Integrated technology for evaluation of brain function and neural plasticity.

The study of neural plasticity has expanded rapidly in the past decades and has shown the remarkable ability of the developing, adult, and aging brain to be shaped by environmental inputs in health and after a lesion. Robust experimental evidence supports the hypothesis that neuronal aggregates adjacent to a lesion in the sensorimotor brain areas can take over progressively the function previously played by the damaged neurons. It definitely is accepted that such a reorganization modifies sensibly the interhemispheric differences in somatotopic organization of the sensorimotor cortices. This reorganization largely subtends clinical recovery of motor performances and sensorimotor integration after a stroke. Brain functional imaging studies show that recovery from hemiplegic strokes is associated with a marked reorganization of the activation patterns of specific brain structures. To regain hand motor control, the recovery process tends over time to bring the bilateral motor network activation toward a more normal intensity/extent, while overrecruiting simultaneously new areas, perhaps to sustain this process. Considerable intersubject variability exists in activation/hyperactivation pattern changes over time. Some patients display late-appearing dorsolateral prefrontal cortex activation, suggesting the development of "executive" strategies to compensate for the lost function. The AH in stroke often undergoes a significant "remodeling" of sensory and motor hand somatotopy outside the "normal" areas, or enlargement of the hand representation. The UH also undergoes reorganization, although to a lesser degree. Although absolute values of the investigated parameters fluctuate across subjects, secondary to individual anatomic variability, variation is minimal with regards to interhemispheric differences, due to the fact that individual morphometric characters are mirrored in the two hemispheres. Excessive interhemispheric asymmetry of the sensorimotor hand areas seems to be the parameter with highest sensitivity in describing brain reorganization after a monohemispheric lesion, and mapping motor and somatosensory cortical areas through focal TMS, fMRI, PET, EEG, and MEG is useful in studying hand representation and interhemispheric asymmetries in normal and pathologic conditions. TMS and MEG allow the detection of sensorimotor areas reshaping, as a result of either neuronal reorganization or recovery of the previously damaged neural network. These techniques have the advantage of high temporal resolution but also have limitations. TMS provides only bidimensional scalp maps, whereas MEG, even if giving three-dimensional mapping of generator sources, does so by means of inverse procedures that rely on the choice of a mathematical model of the head and the sources. These techniques do not test movement execution and sensorimotor integration as used in everyday life. fMRI and PET may provide the ideal means to integrate the findings obtained with the other two techniques. This multitechnology combined approach is at present the best way to test the presence and amount of plasticity phenomena underlying partial or total recovery of several functions, sensorimotor above all. Dynamic patterns of recovery are emerging progressively from the relevant literature. Enhanced recruitment of the affected cortex, be it spared perilesional tissue, as in the case of cortical stroke, or intact but deafferented cortex, as in subcortical strokes, seems to be the rule, a mechanism especially important in early postinsult stages. The transfer over time of preferential activation toward contralesional cortices, as observed in some cases, seems, however, to reflect a less efficient type of plastic reorganization, with some aspects of maladaptive plasticity. Reinforcing the use of the affected side can cause activation to increase again in the affected side with a corresponding enhancement of clinical function. Activation of the UH MI may represent recruitment of direct (uncrossed) corticospinal tracts and relate more to mirror movements, but it more likely reflects activity redistribution within preexisting bilateral, large-scale motor networks. Finally, activation of areas not normally engaged in the dysfunctional tasks, such as the dorsolateral prefrontal cortex or the superior parietal cortex in motor paralysis, might reflect the implication of compensatory cognitive strategies. An integrated approach with technologies able to investigate functional brain imaging is of considerable value in providing information on the excitability, extension, localization, and functional hierarchy of cortical brain areas. Deepening knowledge of the mechanisms regulating the long-term recovery (even if partial), observed for most neurologic sequelae after neural damage, might prompt newer and more efficacious therapeutic and rehabilitative strategies for neurologic diseases.

Animals↗

PubMed2001

Recovery of brain function during induced cerebral hypoperfusion.

We used the setting of clinically indicated internal carotid artery balloon test occlusions in 44 patients with inoperable carotid cavernous aneurysms or head and neck tumours to examine real-time changes in higher cerebral function that correlate with specific levels of cerebral blood flow. By making detailed haemodynamic and neurobehavioural measurements during the 30 min the carotid artery was occluded, we were able to quantify higher cerebral function patterns in relation to absolute cerebral blood flow (CBF) levels. We found that once the carotid artery was occluded, patients whose CBF averaged 47 ml/100 g/min (no different from baseline) maintained consistent performance on a sustained attention task; those whose CBF dropped to an average 37 ml/100 g/min had a reversible deterioration of sustained attention, and those whose CBF fell to 27 ml/100 g/min had impaired sustained attention that persisted until the carotid occlusion was reversed. The relevance of these results to the pathological state of clinical stroke is discussed with respect to the haemodynamic and physiological mechanisms that may determine how brain function is lost and regained in the setting of acute cerebral hypoperfusion.

Attention↗

PubMed1978

Lithium carbonate and brain function. I. Cerebral-evoked potentials, EEG, and symptom changes during lithium carbonate treatment.

Eighteen patients were studied with behavioral ratings and the somatosensory (SER), auditory (AER), and visual (VER) cerebral-evoked response and quantified EEG before and during lithium carbonate treatment. The amplitude of early positive SER components and most AER components increased during treatment, but VER did not change. The intensity of EEG delta and theta frequencies increased, and the dominant alpha frequency slowed. Before treatment, there were few significant correlations to symptom intensity. Patients with an increase in symptoms on treatment had the greatest increase in EEG delta intensity and the dominant alpha frequency slowed in patients who became more depressed. The EEG slowing in patients with a normal sensorium and the change in cerebral cortical activity after transmission in the somatosensory pathway over just three synapses demonstrate a unique and specific effect of lithium carbonate on brain function.

Adult↗

PubMed1982

The effects of diazoxide upon fetal and maternal hemodynamics and fetal brain function and metabolism.

The effects of maternal infusion of Diazoxide (D) were evaluated in two groups of experiments: Nine ewes and their five nonhypoxic fetuses; the remaining four fetuses were excluded because of the development of hypoxia prior to the study. D was directly administered intravenously (IV) to the six fetuses. In group 1 maternal and fetal observations were made at 0, 5, 15, 30, and 45 minutes. A 60-minute observation was also made for the maternal infusion studies. Maternal infusion of 5 mg/kg maternal weight significantly reduced maternal pH from the control value at 5 minutes. Maternal metabolic acidosis was indicated by concomitant significant reductions in base deficit (BD) and total bicarbonate (HCO3), both of which remained low for all subsequent time periods. Maternal lactic acid concentration also increased at 15 minutes, although not significantly. Maternal PO2 also fell significantly at 5 minutes, remaining significantly low for the remaining observations. A profound maternal hypotension was elicited at 5 minutes. All following observations for maternal blood pressure (MBP) were also significantly low. Fetal carotid arterial (FCA) pH declined significantly from the control period value at 15 minutes, remaining significantly low for the remaining observations. FCA O2% saturation (O2%) also witnessed a significant decline from baseline for all observations. FCA serum lactate level rose at 15 minutes; however, this was not deemed significant. No significant changes were seen in fetal brain metabolic rate of oxygen or glucose. Fetal electroencephalogram (EEG) revealed a definite hypoxic change in a majority of cases. In group 2, the effects of a direct fetal IV administration of 30 mg D (mean dose = 7.97 mg/kg fetal weight) were studied in six experiments. No significant changes in fetal acid base status or fetal blood pressure (FBP) were witnessed for the 45 minutes under scrutiny. Fetal heart rate (FHR) showed a short transient rise from baseline at 5 and 15 minutes, returning to normal thereafter. A slight significant decrease in O2% saturation and O2 content were seen only for the 5-minute observation. There were no significant changes of fetal brain function and metabolism observed following D administration to the fetus. The significant fetal hypoxia and acidosis witnessed through the maternal infusion but not in the direct fetal bolus administration were probably owing to profound maternal hypotension resulting in deterioration of uteroplacental perfusion and fetal "gas exchange."

Animals↗