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Spikes Versus BOLD: What Does Neuroimaging Tell Us About Neuronal Activity? David J

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Spikes Versus BOLD: What Does Neuroimaging Tell Us About Neuronal Activity? David J © 2000 Nature America Inc. • http://neurosci.nature.com news and views Spikes versus BOLD: what does neuroimaging tell us about neuronal activity? David J. Heeger, Alex C. Huk, Wilson S. Geisler and Duane G. Albrecht By demonstrating that fMRI responses in human MT+ increase linearly with motion coherence and comparing these responses with slopes of single-neuron firing rates in monkey MT, a new paper provides the best evidence so far that fMRI responses are proportional to firing rates. Functional magnetic resonance imaging to infer something about the changes in signal5, and two recent studies have (fMRI) is a noninvasive technique for mea- underlying neuronal activity. demonstrated a qualitative match .com suring changes in cerebral blood flow and The vascular source of the fMRI sig- between fMRI measurements in human oxygenation that reflect the underlying nal places important limits on the use- visual cortex and multi-unit electrode neuronal activity. This new technology fulness of the technique. At best, the recordings in homologous areas of the offers a powerful method for exploring the fMRI signal (at each image position and macaque monkey cortex6,7. However, the osci.nature neuronal basis of human cognition, per- temporal frame) would be proportional fMRI signal might reflect not only the fir- ception, and behavior, but its ultimate suc- to the local firing rate, averaged over a ing rates of the local neuronal population cess will depend to a large extent on the small region of cortex and a short period but also subthreshold activity, for exam- relationship between the fMRI signal (the of time. If that were true, then it would ple, simultaneous excitation and inhibi- http://neur • blood-oxygenation level dependent or allow us to make direct inferences about tion that would not result in an action BOLD signal) and the underlying spiking firing rates from fMRI data. There is potential but which would nevertheless activity of neurons. Despite the many fMRI some indirect empirical support for a deplete blood oxygen. If that were true, papers appearing in top journals, we still proportional relationship between aver- the interpretation of fMRI data would be have only a rudimentary understanding of age firing rates of neurons and the fMRI confounded. this relationship. Although it is known that the fMRI signal is triggered by oxygen depletion due to the metabolic demands of Motion stimulus 0% Coherence 50% Coherence 100% Coherence increased neuronal activity, the details of 2000 Nature America Inc. this process are only partially under- © stood1–3. In this issue of Nature Neuro- science, Rees et al.4 have taken a major step forward in establishing a quantitative link between neuronal responses and fMRI sig- Responses of nals; their findings offer the most com- pelling support to date for the hypothesis MT neurons that fMRI responses are directly propor- tional to average neuronal firing rates. In a typical fMRI experiment, one col- lects a time-series of images while a stim- ulus or cognitive task is systematically varied. If the stimulus or task variations preferred direction evoke a large enough change in metabol- ic demand in a certain brain region, then Average neuronal the image intensity in that region will response modulate over time about its mean inten- sity value. From these changes, which are typically less than 5%, researchers hope spikes/s David Heeger and Alex Huk are at the Fig. 1. Average firing rate in monkey MT increases linearly with motion coherence. Top, coherent Department of Psychology, Stanford University, motion stimuli. Middle, responses of four hypothetical MT neurons. At 0% coherence (column 1), Stanford, California 94305, USA. Wilson all 4 neurons respond with the same baseline firing rate. At 50% and 100% coherence (columns 2 Geisler and Duane Albrecht are at the and 3), the MT neuron that prefers upward motion increases its firing rate, the responses of neu- Department of Psychology, University of Texas, rons with rightward and leftward preferred directions do not change their firing rates appreciably, Austin, Texas 78712, USA. and the neuron that prefers downward motion decreases its firing rate slightly. Bottom, average e-mail: [email protected] neuronal activity increases linearly with motion coherence. nature neuroscience • volume 3 no 7 • july 2000 631 © 2000 Nature America Inc. • http://neurosci.nature.com news and views Fig. 2. fMRI responses in human 2.8 fits and found that whereas the linear fit V1 are proportional to average 1.0 single neurons accounted for a statistically significant firing rates in monkey V1. Data 2.4 points, human V1 activity as a proportion of the variance in the data, the 0.8 function of stimulus contrast, ctivity 2.0 higher-order polynomials did not fit sig- nal) averaged across subjects and g nificantly better. The reader might be averaged across two different 0.6 1.6 slightly disappointed, however, that the stimulus patterns (adapted from 1.2 graphs in Figs. 4 and 5 of their paper ref. 10). Error bars, ± 1 s.e.m. 0.4 show only the best-fit 3rd-order polyno- fMRI Response fMRI Red curve, average firing rate in BOLD si (% (spikes/s/neuron) 0.8 mials, not the actual measurements of monkey V1, as a function of con- Average Neural A Neural Average 0.2 cortical activity. trast, estimated from a large 0.4 Because of the simple proportional database of microelectrode recordings (333 neurons)11. The 0 0 relationship observed, Rees et al. were ordinates were scaled to obtain 0 10203040506070 able to compare the slopes of the average the best match between the single neuron’s firing rates with their Contrast (%) fMRI responses and the average fMRI data. Assuming that monkey MT firing rates. The average firing rates were determined in the following fashion. Responses as a function and human MT+ are truly homologous of contrast were measured using drifting sine wave gratings of the optimal spatiotemporal frequency, and that firing rates are similar in the two orientation and direction of motion. The responses for each neuron were fitted with a descriptive species, they estimated that a change in function, and the smooth curves were summed across the population. After subtracting the total the fMRI signal of 1% corresponds to a .com maintained activity and dividing by the number of neurons, the average response was then scaled, change in average firing rate of based upon the measured distributions of selectivity of V1 neurons for spatial frequency, temporal fre- quency, orientation and direction of motion11. The average response for the contrast-reversing plaid 9 spikes/second per neuron. patterns used in ref. 10 was determined by adjusting for the differences in spatiotemporal contrast Motivated by this report, we per- between sine waves and contrast-reversing plaids; this adjustment contributed another scaling factor, formed a similar analysis on some of our osci.nature but had almost no effect on the shape of the average contrast response. The average maximum previously reported measurements of the response of V1 neurons in our sample for optimal drifting sine waves is approximately 45 spikes per activity in human and monkey primary second. The relatively low average response rates in Fig. 2 are the result of the high degree of selec- visual cortex (V1). In our fMRI experi- tivity of V1 neurons. A contrast-reversing plaid pattern of a given spatial frequency and orientation ments, we measured human V1 activity http://neur • produces a response in only a small minority of V1 neurons. Therefore, given that most of the cells are as a function of stimulus contrast for a not responding, the average spike rate per neuron for the population as a whole is rather low. particular stimulus pattern10. In our elec- trophysiological experiments, we mea- sured the responses of macaque V1 neurons to stimuli of varying contrasts, Rees and colleagues measured fMRI extensively characterized8,9. Figure 1 (mid- orientations, directions and spatiotem- responses in human MT+ (the MT com- dle) shows the responses of four hypo- poral frequencies11. From this large data- plex, also known as V5), a motion-respon- thetical MT neurons, each with a different base of individual V1 neurons, we sive cortical region that is widely thought preferred motion direction, as a function estimated the average firing rate in mon- 2000 Nature America Inc. to be homologous to monkey cortical areas of motion coherence in the upward direc- key V1, as a function of contrast, for the © MT (also known as V5) and MST. Neurons tion. Across the full range of motion specific stimulus pattern that had been in macaque MT are direction selective; they coherences (from 0% to 100% coherence), used in the fMRI experiments. increase their firing rates when a stimulus the responses of the upward-preferring Our results, like those of Rees et al., moves in a certain ‘preferred’ direction. neuron increase linearly with motion imply a proportional relationship between Their responses are suppressed when the coherence, the responses of the rightward- fMRI response and average firing rate. same stimulus moves opposite to the pre- and leftward-preferring neurons do not The red curve in Fig. 2 represents the aver- ferred direction. Motion in directions change appreciably, and the responses of age neuronal activity (left ordinate), and orthogonal to this axis has little effect on the downward-preferring neuron decrease the data points represent the fMRI mea- the firing rate. Across the population of linearly. Crucially, the slope with which surements (right ordinate). As is evident neurons in MT, different neurons have dif- the upward neuron’s responses increase is in the figure, the two data sets are strik- ferent preferred directions, so that differ- steeper than the slope with which the ingly similar; both increase steeply at low ent directions of motion stimulate different downward neuron’s responses decrease.
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