Nienborg, H. and Cumming, B. G.
Nature, 459:89–92, 2009
DOI, Google Scholar
During perceptual decisions, the activity of sensory neurons correlates with a subject’s percept, even when the physical stimulus is identical. The origin of this correlation is unknown. Current theory proposes a causal effect of noise in sensory neurons on perceptual decisions, but the correlation could result from different brain states associated with the perceptual choice (a top-down explanation). These two schemes have very different implications for the role of sensory neurons in forming decisions. Here we use white-noise analysis to measure tuning functions of V2 neurons associated with choice and simultaneously measure how the variation in the stimulus affects the subjects’ (two macaques) perceptual decisions. In causal models, stronger effects of the stimulus upon decisions, mediated by sensory neurons, are associated with stronger choice-related activity. However, we find that over the time course of the trial these measures change in different directions-at odds with causal models. An analysis of the effect of reward size also supports this conclusion. Finally, we find that choice is associated with changes in neuronal gain that are incompatible with causal models. All three results are readily explained if choice is associated with changes in neuronal gain caused by top-down phenomena that closely resemble attention. We conclude that top-down processes contribute to choice-related activity. Thus, even forming simple sensory decisions involves complex interactions between cognitive processes and sensory neurons.
They investigated the source of the choice probability of early sensory neurons. Choice probability quantifies the difference in firing rate distributions separated by the behavioural response of the subject. The less overlap between the firing rate distributions for one response and its alternative (in two-choice tasks), the greater the choice probability. Importantly, they restricted their analysis to trials in which the stimulus was effectively random. In random dot motion experiments this corresponds to 0% coherent motion, but here they used a disparity discrimination task and looked at disparity selective neurons in macaque area V2. The mean contribution from the stimulus, therefore, should have been 0. Yet, they found that choice probability was above 0.5 indicating that the firing of the neurons still could predict the final response, but why? They consider two possibilities: 1) the particular noise in firing rates of sensory neurons causes, at least partially, the final choice. 2) The firing rate of sensory neurons reflects choice-related effects induced by top-down influences from more decision-related areas.
Note that the choice probability they use is somewhat corrected for influences from the stimulus by considering the firing rate of a neuron in response to a particular disparity, but without taking choices into account. This correction reduced choice probabilities a bit. Nevertheless, they remained significantly above 0.5. This result indicates that the firing rate distributions of the recorded neurons were only little affected by which disparities were shown in individual frames when these distributions are defined depending on the final choice. I don’t find this surprising, because there was no consistent stimulus to detect from the random disparities and the behavioural choices were effectively random.
Yet, the particular disparities presented in individual trials had an influence on the final choice. They used psychophysical reverse correlation to determine this. The analysis suggests that the very first frames had a very small effect which is followed by a steep rise in influence of frames at the beginning of a trial (until about 200ms) and then a steady decline. This result can mean different things depending on whether you believe that evidence accumulation stops once you have reached a threshold, or whether evidence accumulation continues until you are required to make a response. Shadlen is probably a proponent of the first proposition. Then, the decreasing influence of the stimulus on the choice just reflects the smaller number of trials in which the threshold hasn’t been reached, yet. Based on the second proposition, the result means that the weight of individual pieces of evidence during accumulation reduces as you come closer to the response. Currently, I can’t think of decisive evidence for either proposition, but it has been shown in perturbation experiments that stimulus perturbations close to a decision, late in a trial had smaller effects on final choices than perturbations early in a trial (Huk and Shadlen, 2005).
Back to the source of above chance-level choice probabilities. The authors argue, given the decreasing influence of the stimulus on the final choice and assuming that the influence of the stimulus on sensory neurons stays constant, that choice probabilities should also decrease towards the end of a trial. However, choice probabilities stay roughly constant after an initial rise. Consequently, they infer that the firing of the neurons must be influenced from other sources, apart from the stimulus, which are correlated with the choice. They consider two of these sources: i) Lateral, sensory neurons which could reflect the final decision better. ii) Higher, decision related areas which, for example, project a kind of bias onto the sensory neurons. The authors strongly prefer ii), also because they found that the firing of sensory neurons appears to be gain modulated when contrasting firing rates between final choices. In particular, firing rates showed a larger gain (steeper disparity tuning curve of neuron) when trials were considered which ended with the behavioural choice corresponding to the preferred dispartiy of the neuron. In other words, the output of a neuron was selectively increased, if that neuron preferred the disparity which was finally chosen. Equivalently, the output of a neuron was selectively decreased, if that neuron preferred a different disparity than the one which was finally chosen. This gain difference explains at least part of the difference in firing rate distributions which the choice probability measures.
They also show an interesting effect of reward size on the correlation between stimulus and final choice: Stimulus had larger influence on choice for larger reward. Again, if the choice probabilities were mainly driven by stimulus, bottom-up related effects and the stimulus had a larger influence on final choice in high reward trials, then choice probabilities should have been higher in high reward trials. The opposite was the case: choice probabilities were lower in high reward trials. The authors explain this using the previous bias hypothesis: The measured choice probabilities reflect something like an attentional gain or bias induced by higher-level decision-related areas. As the stimulus becomes more important, the bias looses influence. Hence, the choice probabilities reduce.
In summary, the authors present convincing evidence that already sensory neurons in early visual cortex (V2) receive top-down, decision-related influences. Compared with a previous paper (Nienborg and Cumming, 2006) the reported choice probabilities here were quite similar to those reported there, even though here only trials with complete random stimuli were considered. I would have guessed that choice probabilities would be considerably higher for trials with an actually presented stimulus. Why is there only a moderate difference? Perhaps there actually isn’t. My observation is only based on a brief look at the figures in the two papers.