Neural correlates of perceptual learning in a sensory-motor, but not a sensory, cortical area

In the paper

“Behavioural sensitivity to weak motion signals improved continuously during training, long after monkeys had acquired the stimulus/response association.”

In the paper

“During training, improved behavioural sensitivity to weak motion signals was accompanied by changes in motion-driven responses of neurons in LIP but not MT.”

• Also stated in: § Abstract · plain

  “This improvement in behavioural sensitivity corresponded to changes in the responses of neurons in LIP but not MT during motion viewing.”

In the paper

“The time course and magnitude of the changes in LIP were correlated with the changes in behavioural sensitivity throughout training.”

• Also stated in: § Results · plain

  “Moreover, LIP activity was correlated with behavioural threshold across sessions after taking into account the high-coherence errors (Fig. 5, left; partial correlation rth,(k3|λ) = −0.42, H0: r=0 using Fisher’s Z transformation, p<10−5 for monkey C; rth,(k3|λ) =−0.35, p=0.0049 for monkey Z)”

In the paper

“Behavioural performance improved steadily for both monkeys with training (Fig. 2).”

In the paper

“Interestingly, this lack of long-term changes across sessions occurred despite short-term changes within sessions, as has been reported previously (geometric mean±SEM ratio of psychometric thresholds in the second 200 versus the first 200 trials = 0.92±0.22 in monkey C and 0.84±0.29 in monkey Z; ratio of neurometric thresholds in MT in the second 200 versus the first 200 trials = 0.87±0.23 in monk”

What the sources say

• Not checked yetcites [30] Zohary, E., Celebrini, S., Britten, K.H. & Newsome, W.T. Neuronal plasticity that underlies improvement in perceptual performance. Science 263, 1289–1292 (1994). source

In the paper

“There was, however, a slight strengthening of the relationship between the trial-by-trial variability of MT responses and the monkeys’ choices with training.”

In the paper

“Moreover, none of the three terms changed significantly with training (linear regression versus session, computed separately for each term, each monkey and before and during training, H0: slope=0, p>0.05 for all conditions).”

In the paper

“This specificity for the axis of motion was mirrored in neural activity in LIP (Fig. 7b, red symbols; monkey C: r=−0.37, p=0.0004; monkey Z: r=−0.29, p=0.0204) but not MT (Fig. 7b, cyan symbols; monkey C: r=0.09, p=0.5439; monkey Z: r=0.22, p=0.2063)”

In the paper

“However, responses of the most sensitive MT neurons became increasingly predictive of the monkeys’ choices with training.”

In the paper

“On trials in which the other target was selected, LIP activity tended to decrease gradually during motion viewing and then remain below baseline levels until after the saccade.”

In the paper

“Other response properties including the width of directional tuning were unaffected by training (Table S1 and Fig. S3).”

In the paper

“A larger effect was seen in the coherence × time interaction term, which began near zero and thus indicated little or no influence of the motion stimulus on the LIP responses at the beginning of training, and progressed steadily to more positive values.”

In the paper

“Moreover, the relationship between choice probability and motion sensitivity in MT changed systematically over the course of training such that more sensitive neurons became more predictive of the monkey’s direction decision as training progressed (Fig. 3c; correlation coefficient between choice probability and neurometric thresholds of MT neurons in the 1st 1/3 sessions, r=0.02, H0: r=0, p=0.5600”

In the paper

“but the converse was not true, with no correlation between high-coherence errors and LIP activity after taking into account the changes in behavioural threshold (rλ,(k3|th) =0.0460, p=0.6198 for monkey C; rλ,(k3|th)= −0.0590, p=0.6011 for monkey Z).”

In the paper

“For both monkeys, discrimination performance depended on the familiarity of the axis of motion (Fig. 7).”

In the paper

“Our results show that for monkeys trained to discriminate the direction of motion of noisy visual stimuli, improvements in discrimination threshold (i.e., higher sensitivity to weak motion) corresponded to changes in sensory-driven responses in area LIP but not MT.”

In the paper

“For both monkeys, the coherence- and time-alone terms tended to be near zero throughout training (although the coherence term decreased slightly to small negative values with training in both monkeys, and the time term increased slightly to small positive values with training in monkey C).”

In the paper

“As illustrated in Fig. 3a, MT responses before and during training showed a pattern of activation similar to that reported in trained monkeys16: motion in the preferred direction elicited an increase in spike rate and motion in the opposite direction elicited a decrease in spike rate to relatively constant values that depended on motion strength and sustained throughout motion viewing.”

What the sources say

• Not checked yetcites [16] Britten, K.H., Shadlen, M.N., Newsome, W.T. & Movshon, J.A. The analysis of visual motion: a comparison of neuronal and psychophysical performance. J. Neurosci. 12, 4745–4765 (1992). source

In the paper

“Other behavioural parameters including the shape and time dependence of the psychometric function did not show similar systematic changes with training (Table S1).”

In the paper

“Choice probability increased as a function of training session (combined data from both monkeys, mean±SEM choice probability = 0.493±0.011 for the first 30% and 0.549±0.018 for the last 30% of sessions).”

In the paper

“For both monkeys, the value of this quantity was negatively correlated with the absolute z score of motion direction (monkey C: correlation coefficients r=−0.39, H0: r=0 using Fisher’s Z transformation p<10−7; monkey Z: r=−0.49, p<10−9), indicating that performance tended to degrade when an unfamiliar stimulus was used.”

In the paper

“For both monkeys, only the coherence-alone term was typically >0, consistent with the idea that MT responses provide evidence about motion direction that depends only on stimulus strength and not viewing time.”

In the paper

“In addition to learning the association, the monkeys learned to better discriminate weaker and weaker motion signals at shorter viewing times.”

In the paper

“In LIP, neurons tuned for saccadic direction were insensitive to visual motion at the beginning of training but developed responses that grew increasingly strongly with motion strength and viewing time as performance on the task improved.”

In the paper

“Moreover, the neurometric thresholds of neither the whole population nor the 50% most sensitive MT neurons changed systematically as a function of session either before or during training (linear regression, H0: slope of log threshold versus session=0; before training: monkey C, p=0.7612; monkey Z, p=0.9507, during training: monkey C, whole population, p=0.9498, 50% most sensitive, p=0.9899;”

In the paper

“we found that motion-driven LIP responses appeared when the monkeys learned the association between motion direction and saccadic response.”

In the paper

“we found no evidence for such modulation by numerous oculomotor and motivational parameters.”

In the paper

“Thus, for this task, perceptual learning appears to involve improvements not in how sensory information is represented in the brain but rather how the sensory representation is interpreted to form the decision that guides behaviour.”

• Also stated in: § Abstract · hedged

  “The results are consistent with a model in which perceptual improvements result from changes in how sensory evidence is interpreted and used to instruct behaviour, as reflected in LIP, but not in changes to the representation of the evidence itself in MT.”

• Also stated in: § Results · hedged

  “Our results suggest that the improvements in behavioural sensitivity result from changes not in the sensory representation but rather its interpretation.”

In the paper

“Thus, MT provides at least some of the motion information used to form the direction decision.”

What the sources say

• Not checked yetcites [16] Britten, K.H., Shadlen, M.N., Newsome, W.T. & Movshon, J.A. The analysis of visual motion: a comparison of neuronal and psychophysical performance. J. Neurosci. 12, 4745–4765 (1992). source
• Not checked yetcites [17] Britten, K.H., Newsome, W.T., Shadlen, M.N., Celebrini, S. & Movshon, J.A. A relationship between behavioral choice and the visual responses of neurons in macaque MT. Vis. Neurosci. 13, 87–100 (1996). source
• Not checked yetcites [18] Newsome, W.T. & Pare, E.B. A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J. Neurosci. 8, 2201–2211 (1988). source
• Not checked yetcites [19] Salzman, C.D., Britten, K.H. & Newsome, W.T. Cortical microstimulation influences perceptual judgments of motion direction. Nature 346, 174–177 (1990). source

In the paper

“Thus, LIP appears to play a role in transforming motion information into a saccadic choice, although that role might be shared among several oculomotor regions including the frontal eye field and superior colliculus that show similar responses during task performance27, 28.”

What the sources say

• Not checked yetcites [24] Shadlen, M.N. & Newsome, W.T. Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. J. Neurophysiol. 86, 1916–1936 (2001). source
• Not checked yetcites [25] Roitman, J.D. & Shadlen, M.N. Response of neurons in the lateral intraparietal area during a combined visual discrimination reaction time task. J. Neurosci. 22, 9475–9489 (2002). source
• Not checked yetcites [26] Hanks, T.D., Ditterich, J. & Shadlen, M.N. Microstimulation of macaque area LIP affects decision-making in a motion discrimination task. Nat. Neurosci. 9, 682–689 (2006). source

In the paper

“However, monkeys trained on visual tasks show only moderate or no change in early visual cortex7–11.”

What the sources say

• Not checked yetcites [7] Schoups, A., Vogels, R., Qian, N. & Orban, G. Practicing orientation identification improves orientation coding in V1 neurons. Nature 412, 549–553 (2001). source
• Not checked yetcites [8] Crist, R.E., Li, W. & Gilbert, C.D. Learning to see: experience and attention in primary visual cortex. Nat. Neurosci. 4, 519–525 (2001). source
• Not checked yetcites [9] Ghose, G.M., Yang, T. & Maunsell, J.H. Physiological correlates of perceptual learning in monkey V1 and V2. J. Neurophysiol. 87, 1867–1888 (2002). source
• Not checked yetcites [10] Yang, T. & Maunsell, J.H. The effect of perceptual learning on neuronal responses in monkey visual area V4. J. Neurosci. 24, 1617–1626 (2004). source
• Not checked yetcites [11] Raiguel, S., Vogels, R., Mysore, S.G. & Orban, G.A. Learning to see the difference specifically alters the most informative V4 neurons. J. Neurosci. 26, 6589–6602 (2006). source

In the paper

“electrophysiological studies in monkeys that found little or no changes in V1 with perceptual learning7–9”

What the sources say

• Not checked yetcites [7] Schoups, A., Vogels, R., Qian, N. & Orban, G. Practicing orientation identification improves orientation coding in V1 neurons. Nature 412, 549–553 (2001). source
• Not checked yetcites [8] Crist, R.E., Li, W. & Gilbert, C.D. Learning to see: experience and attention in primary visual cortex. Nat. Neurosci. 4, 519–525 (2001). source
• Not checked yetcites [9] Ghose, G.M., Yang, T. & Maunsell, J.H. Physiological correlates of perceptual learning in monkey V1 and V2. J. Neurophysiol. 87, 1867–1888 (2002). source

In the paper

“The changes in sensory-driven LIP responses reflected the improvements in behavioural sensitivity to weak motion signals.”

In the paper

“the motion sensitivity of MT neurons likely arises from their direct and indirect input from V135”

What the sources say

• Not checked yetcites [35] Movshon, J.A. & Newsome, W.T. Visual response properties of striate cortical neurons projecting to area MT in macaque monkeys. J. Neurosci. 16, 7733–7741 (1996). source

In the paper

“our results appear to rule out learning-induced changes in V1, as well.”

In the paper

“The changes in sensory-driven LIP responses with training also did not appear to reflect changes in other motor (Fig. 5, middle) or motivational parameters (Fig. 5, right) known to modulate LIP activity21, 22.”

What the sources say

• Not checked yetcites [21] Platt, M.L. & Glimcher, P.W. Neural correlates of decision variables in parietal cortex. Nature 400, 233–238 (1999). source
• Not checked yetcites [22] Snyder, L.H., Batista, A.P. & Andersen, R.A. Intention-related activity in the posterior parietal cortex: a review. Vision Res. 40, 1433–1441 (2000). source

In the paper

“For both monkeys, only the coherence-alone term was typically >0, consistent with the idea that MT responses provide evidence about motion direction that depends only on stimulus strength and not viewing time.”

In the paper

“provides additional evidence that the stimulus specificity of perceptual learning does not necessarily imply changes in primary sensory cortex3, 4.”

What the sources say

• Not checked yetcites [3] Mollon, J.D. & Danilova, M.V. Three remarks on perceptual learning. Spat. Vis. 10, 51–58 (1996). source
• Not checked yetcites [4] Dosher, B.A. & Lu, Z.L. Mechanisms of perceptual learning. Vision Res. 39, 3197–3221 (1999). source

In the paper

“Thus, the systematic change in choice probability is likely to reflect an increasingly selective read-out of activity from MT neurons, particularly those most sensitive to the motion stimulus.”

In the paper

“The results suggest that the perceptual improvements corresponded to an increasingly selective read-out of highly sensitive MT neurons by a decision process, represented in LIP, that instructed the behavioural response.”

In the paper

“The results also further support a close relationship between learning and attention12.”

What the sources say

• Not checked yetcites [12] Ahissar, M. & Hochstein, S. Attentional control of early perceptual learning. Proc. Natl. Acad. Sci. USA 90, 5718–5722 (1993). source

In the paper

“Learned sensory-motor associations have been shown to correspond to changes in LIP but not MT41, 42.”

What the sources say

• Not checked yetcites [41] Freedman, D.J. & Assad, J.A. Experience-dependent representation of visual categories in parietal cortex. Nature 443, 85–88 (2006). source
• Not checked yetcites [42] Grunewald, A., Linden, J.F. & Andersen, R.A. Responses to auditory stimuli in macaque lateral intraparietal area. I. Effects of training. J. Neurophysiol. 82, 330–342 (1999). source

In the paper

“These decision computations represented in LIP appear to be critical for performance of trained monkeys, an idea supported by a close relationship between LIP responses and reaction times25 and the ability to bias performance using electrical microstimulation of LIP26.”

What the sources say

• Not checked yetcites [25] Roitman, J.D. & Shadlen, M.N. Response of neurons in the lateral intraparietal area during a combined visual discrimination reaction time task. J. Neurosci. 22, 9475–9489 (2002). source
• Not checked yetcites [26] Hanks, T.D., Ditterich, J. & Shadlen, M.N. Microstimulation of macaque area LIP affects decision-making in a motion discrimination task. Nat. Neurosci. 9, 682–689 (2006). source

In the paper

“These results support the intriguing possibility that associative and perceptual learning might share common mechanisms4, 43.”

What the sources say

• Not checked yetcites [4] Dosher, B.A. & Lu, Z.L. Mechanisms of perceptual learning. Vision Res. 39, 3197–3221 (1999). source
• Not checked yetcites [43] Hall, G. Perceptual and Associative Learning (Oxford University Press, Oxford, 1991). source

In the paper

“our recording and analysis methods could resolve within-session changes in MT sensitivity30 that were smaller in magnitude than the longer-term changes that we would expect based on behaviour.”

What the sources say

• Not checked yetcites [30] Zohary, E., Celebrini, S., Britten, K.H. & Newsome, W.T. Neuronal plasticity that underlies improvement in perceptual performance. Science 263, 1289–1292 (1994). source

In the paper

“the sensory-driven LIP responses changed in a manner that was consistent with a decision process that used increasingly sensitive motion evidence to determine the saccadic choice.”

In the paper

“primary somatosensory and auditory cortices, which in both monkeys and humans can show dramatic changes with perceptual learning5, 6, 37–39.”

What the sources say

• Not checked yetcites [5] Recanzone, G.H., Schreiner, C.E. & Merzenich, M.M. Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J. Neurosci. 13, 87–103 (1993). source
• Not checked yetcites [6] Recanzone, G.H., Merzenich, M.M., Jenkins, W.M., Grajski, K.A. & Dinse, H.R. Topographic reorganization of the hand representation in cortical area 3b owl monkeys trained in a frequency-discrimination task. J. Neurophysiol. 67, 1031–1056 (1992). source
• Not checked yetcites [37] Pleger, B. et al. Functional imaging of perceptual learning in human primary and secondary somatosensory cortex. Neuron 40, 643–653 (2003). source
• Not checked yetcites [38] Bao, S., Chang, E.F., Woods, J. & Merzenich, M.M. Temporal plasticity in the primary auditory cortex induced by operant perceptual learning. Nat. Neurosci. 7, 974–981 (2004). source
• Not checked yetcites [39] Blake, D.T., Heiser, M.A., Caywood, M. & Merzenich, M.M. Experience-dependent adult cortical plasticity requires cognitive association between sensation and reward. Neuron 52, 371–381 (2006). source

In the paper

“Our results are consistent with such a refinement of direct or indirect ascending projections from MT to LIP44, an idea that merits further testing.”

What the sources say

• Not checked yetcites [44] Lewis, J.W. & Van Essen, D.C. Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. J. Comp. Neurol. 428, 112–137 (2000). source