Representation of accumulating evidence for a decision in two parietal areas

“The reported latencies are the times at which the ROC index significantly departed from 0.5 for at least 50 ms ( p 0.05; Hanley and McNeil, 1982).”

“Experimental control and stimulus presentation were achieved with either REX (Hays et al., 1982) in combination with the Psychophysics toolbox (Brainard, 1997) or with EXPO (developed by Peter Lennie, currently maintained by Rod Dotson, Center for Neural Science at New York University, New York,…”

“This is not the type of parallel processing that is often associated with neural networks (Rumelhart and McClelland, 1986) or computer systems but is instead a direct representation (Barlow, 1995) of a decision variable in the firing rates of neurons.”

“Such an accumulation of noisy evidence has been likened to a random walk or diffusion process (Ratcliff, 1978; Gold and Shadlen, 2002).”

“…occurs in circuits associated with provisional behavioral responses to stim- uli (Schall, 2001; Romo et al., 2004; Rorie and Newsome, 2005; Gold and Shadlen, 2007; Lemus et al., 2007; Andersen and Cui, 2009; Cisek and Kalaska, 2010; Hernández et al., 2010; Westendorff et al., 2010),…”

“We estimated the rate of this rise or decline by fitting lines to the response averages in the 150 ms epoch from the earliest point that these trends appear to emerge (see Materials and Methods).”

“…saccadic eye movements (Thier and Andersen, 1998), MIP neurons signal the spatial location of objects that are potential targets of reach movements (Mountcastle et al., 1975; Johnson et al., 1996; Snyder et al., 1997; Batista et al., 1999; Eskandar and Assad, 1999), as well as the outcome of…”

“We recorded from single neurons in areas LIP and MIP of two rhesus monkeys that were trained to judge the direction of motion of a dynamic random-dot display (Britten et al., 1992).”

“We also fit a bounded drift-diffusion model (Ratcliff, 1978; Gold and Shadlen, 2002; Bogacz et al., 2006) to account for the variation in choice accuracy as a function of the duration, strength, and direction of random-dot motion (Fig.”

“7, insets), consistent with the hypothesis that the firing rates represent the accumulated difference in motion evidence from opposing pools of motion-sensing neurons, such as those in middle temporal area MT (Shadlen and Newsome, 1996, 2001; Mazurek et al., 2003; Huk and Shadlen, 2005).”

“…of motion in a dynamic random-dot display, neural correlates of evidence accumulation (Shadlen and Newsome, 1996; Huk and Shadlen, 2005), value (Platt and Glimcher, 1999; Rorie et al., 2010), probability (Yang and Shadlen, 2007), and confidence (Kiani and Shadlen, 2009) have been identified in…”

“, 2004) and also as reflecting covert eye movements that might occur were the monkeys not required to hold fixation away from the reach target (Snyder et al., 1997, 1998; Colby and Goldberg, 1999).”

“…in LIP and other oculomotor areas suggests that the motor system is not recruited once a decision is made but instead receives a continuous flow of partial information—an evolving decision variable (Gold and Shadlen, 2007; McKinstry et al., 2008; Cisek and Kalaska, 2010; Selen et al., 2012).”

“…a sign of allocation of spatial attention (Robinson et al., 1978; Bushnell et al., 1981; Wardak et al., 2004) and also as reflecting covert eye movements that might occur were the monkeys not required to hold fixation away from the reach target (Snyder et al., 1997, 1998; Colby and Goldberg, 1999).”

“, 2010), probability (Yang and Shadlen, 2007), and confidence (Kiani and Shadlen, 2009) have been identified in the firing rates of neurons in the parietal and prefrontal association cortex and in subcortical structures associated with the preparation of eye movements (Horwitz and Newsome, 1999).”

“The random-dot motion task is useful for studying this process because (1) its solution requires integration of evidence across space and time and (2) a neural representation of the momentary evidence has been established in areas MT and MST (Salzman et al., 1990; Celebrini and Newsome, 1994; Ditterich et al., 2003).”

“Together, these analyses allow us to appreciate that the firing rate functions plotted in Figure 7 are the means of diffusion paths, as predicted by the drift-diffusion model (Link, 1975; Ratcliff, 1978; Gold and Shadlen, 2001).”

“The recruitment of saccade-related neurons during reach movements has been interpreted in the past as a sign of allocation of spatial attention (Robinson et al., 1978; Bushnell et al., 1981; Wardak et al., 2004) and also as reflecting covert eye movements that might occur were the monkeys not required to hold fixation…”

“The recruitment of saccade-related neurons during reach movements has been interpreted in the past as a sign of allocation of spatial attention (Robinson et al., 1978; Bushnell et al., 1981; Wardak et al., 2004) and also as reflecting covert eye movements that might occur were the monkeys not required to hold fixation…”

“7, insets), consistent with the hypothesis that the firing rates represent the accumulated difference in motion evidence from opposing pools of motion-sensing neurons, such as those in middle temporal area MT (Shadlen and Newsome, 1996, 2001; Mazurek et al., 2003; Huk and Shadlen, 2005).”

“…the spatial location of objects that are potential targets of reach movements (Mountcastle et al., 1975; Johnson et al., 1996; Snyder et al., 1997; Batista et al., 1999; Eskandar and Assad, 1999), as well as the outcome of decisions to direct the arm in a particular direction (Snyder et al.,…”

“…provisional behavioral responses to stim- uli (Schall, 2001; Romo et al., 2004; Rorie and Newsome, 2005; Gold and Shadlen, 2007; Lemus et al., 2007; Andersen and Cui, 2009; Cisek and Kalaska, 2010; Hernández et al., 2010; Westendorff et al., 2010), which has been termed an intentional—as…”

“…and Andersen, 1998), MIP neurons signal the spatial location of objects that are potential targets of reach movements (Mountcastle et al., 1975; Johnson et al., 1996; Snyder et al., 1997; Batista et al., 1999; Eskandar and Assad, 1999), as well as the outcome of decisions to direct the arm in…”

“…and not about the plan of action used to communicate the choice, yet our decisions are governed by an evidence accumulation process similar to the one studied in monkeys (Smith and Ratcliff, 2004; Palmer et al., 2005; Philiastides et al., 2006; Green et al., 2012; O’Connell et al., 2012).”

“…of these fluctuations on the monkeys’ choices, we extracted the motion energy profile (Adelson and Bergen, 1985; Neri, 2004; Kiani et al., 2008; Resulaj et al., 2009) as a function of time from the dis- play of each trial, applying a sign convention such that positive motion energy represents…”

“7, insets), consistent with the hypothesis that the firing rates represent the accumulated difference in motion evidence from opposing pools of motion-sensing neurons, such as those in middle temporal area MT (Shadlen and Newsome, 1996, 2001; Mazurek et al., 2003; Huk and Shadlen, 2005).”

“…of evidence accumulation (Shadlen and Newsome, 1996; Huk and Shadlen, 2005), value (Platt and Glimcher, 1999; Rorie et al., 2010), probability (Yang and Shadlen, 2007), and confidence (Kiani and Shadlen, 2009) have been identified in the firing rates of neurons in the parietal and prefrontal…”

“In particular, LIP is known to represent the accumulated evidence, combined with other factors that affect the decision, such as the previous probability, value, and costs associated with the alternatives (Seo et al., 2009; Rorie et al., 2010; Hanks et al., 2011; Drugowitsch et al., 2012).”

“7, insets), consistent with the hypothesis that the firing rates represent the accumulated difference in motion evidence from opposing pools of motion-sensing neurons, such as those in middle temporal area MT (Shadlen and Newsome, 1996, 2001; Mazurek et al., 2003; Huk and Shadlen, 2005).”

“…areas supports the idea that analysis of sensory information occurs in circuits associated with provisional behavioral responses to stim- uli (Schall, 2001; Romo et al., 2004; Rorie and Newsome, 2005; Gold and Shadlen, 2007; Lemus et al., 2007; Andersen and Cui, 2009; Cisek and Kalaska,…”

“To quantify the influence of these fluctuations on the monkeys’ choices, we extracted the motion energy profile (Adelson and Bergen, 1985; Neri, 2004; Kiani et al., 2008; Resulaj et al., 2009) as a function of time from the dis- play of each trial, applying a sign convention such that positive…”

“, 1999; Eskandar and Assad, 1999), as well as the outcome of decisions to direct the arm in a particular direction (Snyder et al., 1997; Eskandar and Assad, 1999; Scherberger and Andersen, 2007; Pesaran et al., 2008).”

“…and not about the plan of action used to communicate the choice, yet our decisions are governed by an evidence accumulation process similar to the one studied in monkeys (Smith and Ratcliff, 2004; Palmer et al., 2005; Philiastides et al., 2006; Green et al., 2012; O’Connell et al., 2012).”

“In particular, LIP is known to represent the accumulated evidence, combined with other factors that affect the decision, such as the previous probability, value, and costs associated with the alternatives (Seo et al., 2009; Rorie et al., 2010; Hanks et al., 2011; Drugowitsch et al., 2012).”

“We then combined the residuals and their associated means using Equation 6 from the study by Churchland et al. (2011) to estimate the VarCE, S Ni 2 , in the six time bins under the four conditions (area by effector), given .”

“…supports the idea that analysis of sensory information occurs in circuits associated with provisional behavioral responses to stim- uli (Schall, 2001; Romo et al., 2004; Rorie and Newsome, 2005; Gold and Shadlen, 2007; Lemus et al., 2007; Andersen and Cui, 2009; Cisek and Kalaska, 2010; Hernández…”

“The random-dot motion task is useful for studying this process because (1) its solution requires integration of evidence across space and time and (2) a neural representation of the momentary evidence has been established in areas MT and MST (Salzman et al., 1990; Celebrini and Newsome, 1994; Ditterich et al., 2003).”

“…its decision with an eye movement, a neural representation of the accumulated evidence has been demonstrated in area LIP, the frontal eye fields, the superior colliculus, and the dorsolateral prefrontal cortex (Horwitz and Newsome, 1999; Gold and Shadlen, 2000, 2007; Ding and Gold, 2012).”

“Moreover, the accumulating sensory evidence that will ultimately support one or the other choice—an evolving decision variable— has been shown to flow continuously to motor structures in the human brain much as it does in monkeys (McKinstry et al., 2008; Selen et al., 2012; Ding and Gold, 2013).”

“…its decision with an eye movement, a neural representation of the accumulated evidence has been demonstrated in area LIP, the frontal eye fields, the superior colliculus, and the dorsolateral prefrontal cortex (Horwitz and Newsome, 1999; Gold and Shadlen, 2000, 2007; Ding and Gold, 2012).”

“The random-dot motion task is useful for studying this process because (1) its solution requires integration of evidence across space and time and (2) a neural representation of the momentary evidence has been established in areas MT and MST (Salzman et al., 1990; Celebrini and Newsome, 1994; Ditterich et al., 2003).”

“Just as LIP neurons signal the location of objects that are potential objects of saccadic eye movements (Thier and Andersen, 1998), MIP neurons signal the spatial location of objects that are potential targets of reach movements (Mountcastle et al.”

“…of objects that are potential targets of reach movements (Mountcastle et al., 1975; Johnson et al., 1996; Snyder et al., 1997; Batista et al., 1999; Eskandar and Assad, 1999), as well as the outcome of decisions to direct the arm in a particular direction (Snyder et al., 1997; Eskandar and Assad,…”

“Moreover, the accumulating sensory evidence that will ultimately support one or the other choice—an evolving decision variable— has been shown to flow continuously to motor structures in the human brain much as it does in monkeys (McKinstry et al., 2008; Selen et al., 2012; Ding and Gold, 2013).”

“Moreover, the accumulating sensory evidence that will ultimately support one or the other choice—an evolving decision variable— has been shown to flow continuously to motor structures in the human brain much as it does in monkeys (McKinstry et al., 2008; Selen et al., 2012; Ding and Gold, 2013).”

“In monkeys trained to discriminate the direction of motion in a dynamic random-dot display, neural correlates of evidence accumulation (Shadlen and Newsome, 1996; Huk and Shadlen, 2005), value (Platt and Glimcher, 1999; Rorie et al., 2010), probability (Yang and Shadlen, 2007), and confidence (Kiani and Shadlen, 2009)…”

“…during reach movements has been interpreted in the past as a sign of allocation of spatial attention (Robinson et al., 1978; Bushnell et al., 1981; Wardak et al., 2004) and also as reflecting covert eye movements that might occur were the monkeys not required to hold fixation away from the reach…”

“…a sign of allocation of spatial attention (Robinson et al., 1978; Bushnell et al., 1981; Wardak et al., 2004) and also as reflecting covert eye movements that might occur were the monkeys not required to hold fixation away from the reach target (Snyder et al., 1997, 1998; Colby and Goldberg, 1999).”

“, 1999; Eskandar and Assad, 1999), as well as the outcome of decisions to direct the arm in a particular direction (Snyder et al., 1997; Eskandar and Assad, 1999; Scherberger and Andersen, 2007; Pesaran et al., 2008).”

“It is also important to note that our experiments were not designed to test effector specificity, and our results might be specific to LIPv and anterior MIP (Liu et al., 2010).”

“In particular, LIP is known to represent the accumulated evidence, combined with other factors that affect the decision, such as the previous probability, value, and costs associated with the alternatives (Seo et al., 2009; Rorie et al., 2010; Hanks et al., 2011; Drugowitsch et al., 2012).”

“The model, which assumes perfect integration of evidence to a threshold or bound, has been shown to account for the rate of improvement in accuracy as a function of both variables (Kiani et al., 2008; Tsetsos et al., 2012).”

“Indeed, careful reading of studies that support motor specialization (Snyder et al., 1997; Cui and Andersen, 2011) attests to only a relative preference for modality, as these investigators have emphasized (Andersen and Cui, 2009).”

“The absence of a visual response to the onset of visual targets is consistent with the anterior location of our recordings in MIP, possibly at the border of MIP/5v (Hwang et al., 2012).”

“…analysis of sensory information occurs in circuits associated with provisional behavioral responses to stim- uli (Schall, 2001; Romo et al., 2004; Rorie and Newsome, 2005; Gold and Shadlen, 2007; Lemus et al., 2007; Andersen and Cui, 2009; Cisek and Kalaska, 2010; Hernández et al., 2010;…”

“…2004; Rorie and Newsome, 2005; Gold and Shadlen, 2007; Lemus et al., 2007; Andersen and Cui, 2009; Cisek and Kalaska, 2010; Hernández et al., 2010; Westendorff et al., 2010), which has been termed an intentional—as opposed to representational—framework for information processing (Shadlen et…”

“…associated with provisional behavioral responses to stim- uli (Schall, 2001; Romo et al., 2004; Rorie and Newsome, 2005; Gold and Shadlen, 2007; Lemus et al., 2007; Andersen and Cui, 2009; Cisek and Kalaska, 2010; Hernández et al., 2010; Westendorff et al., 2010), which has been termed an…”

“To quantify the influence of these fluctuations on the monkeys’ choices, we extracted the motion energy profile (Adelson and Bergen, 1985; Neri, 2004; Kiani et al., 2008; Resulaj et al., 2009) as a function of time from the dis- play of each trial, applying a sign convention such that positive…”

“…and not about the plan of action used to communicate the choice, yet our decisions are governed by an evidence accumulation process similar to the one studied in monkeys (Smith and Ratcliff, 2004; Palmer et al., 2005; Philiastides et al., 2006; Green et al., 2012; O’Connell et al., 2012).”

“…formally identical to evidence accumulation described by drift diffusion or race-to-bound models (Solway & Botvinick, 2012; Zhang & Maloney, 2012; de Lafuente et al., 2015; Kira et al., 2015) and nicely recapitulates the emergence of a choice as evaluation of options proceeds (Hunt et al., 2012).”

“This formulation also has some construct validity in relation to theoretical proposals and empirical work on evidence accumulation (de Lafuente, Jazayeri, & Shadlen, 2015; Kira, Yang, & Shadlen, 2015) and the neuronal encoding of probabilities (Deneve, 2008).”

“Movements with fine temporal structure, cognitive functions such as deliberation and integration (de Lafuente et al., 2015; Hanks et al., 2015;Merchant and Georgopoulos, 2006; Roitman and Shadlen, 2002; Shadlen and Gold, 2004; Thura and Cisek, 2014), and behaviors that depend on knowledge of…”

“, [74]) In many of the decisions subjects face in their daily life, LIP, in fact, may not have a role at all.”

“Moreover, decision-related activity has been shown to occur in parallel in areas associated with different motor responses (44-46).”

“…activity that discriminates the categorical alternatives even when the appropriate stimulus– response mapping is withheld until a response cue (Freedman and Assad, 2006; Bennur and Gold, 2011) or when hand movements are used to report decisions instead of saccades (de Lafuente et al., 2015).”

“Interestingly, during accumulation of decision variables, neural activity in LIP is modulated when the decision outcome is not only a saccade, but also a reaching movement (de Lafuente et al., 2015).”

“These areas include the frontal eye fields (Ding & Gold 2012a, Gold & Shadlen 2000, Kim & Shadlen 1999), the parietal reach region (de Lafuente et al. 2015), and subcortical structures such as the superior colliculus (Horwitz & Newsome 1999) and the caudate nucleus (Ding & Gold 2010, 2012b).”

“This is surprising, but it could be explained by lack of power—a combination of small numbers of M in neurons, narrow sample windows (50 ms boxcar) and the focus on the long RT trials.”

“This question can be answered with tasks in which subjects report the outcome of the same sensory discrimination through different motor actions (78, 79, 85–87).”

“Consistent with this interpretation, there is overwhelming evidence for decision-related responses in primate oculomotor brain areas (de Lafuente et al., 2015; Shadlen and Newsome, 1996), and such responses are thought to drive eye movements (Joo et al., 2016).”

“Presumably, the decision to report and the decision to move are not the same process, just as the decision to report with a saccade or a reach movement is subserved by different circuits [27, 28].”

“…brain areas associated with operantly-conditioned motor responses in sensorimotor decision-making processes leading to action choices (Brody and Hanks, 2016; de Lafuente et al., 2015; Glimcher, 2001; Huda et al., 2018; Roitman and Shadlen, 2002; Romo et al., 2004; Shadlen and Newsome, 1996).”

“We first established the presence of firing-rate encoding of choice and the temporal structure of the neuronal activity in the PPC (11, 32, 35) before testing whether and how decision coding varies with the temporal structure of neuronal activity.”

“…over time (e.g. random dot kinematograms) (de Bruyn & Orban, 1988; Glass & Pérez, 1973; Snowden & Braddick, 1990; Watanabe & Kikuchi, 2006; de Lafuente et al., 2015; Gold & Shadlen, 2000; Kim & Shadlen, 1999; Liu & Pleskac, 2011; Drugowitsch et al., 2015; Gu et al., 2008; Hou et al.,…”

“It has been especially useful as a signature of neural computations related to temporal accumulation in the context of decision making (Churchland et al. 2011; de Lafuente et al. 2015; Marcos et al. 2013).”

“For example, the representation of an object relative to the hand could be achieved in parietal cortex using neurons that represent hand displacement in an oculocentric FoR (see Snyder et al., 1997; Batista, 1999; de Lafuente et al., 2015; Stuphorn et al., 2000).”

“…suggest that differences in dyslexia arise because of the efficiency with which evidence is extracted from global motion stimuli and integrated toward a decision bound, which is often attributed to parietal areas (Shadlen and Newsome, 1996, 2001; Hanks et al., 2006; de Lafuente et al., 2015).”

“Future work could also investigate whether children ’ s responses may be captured better by models which incorporate urgency signals or collapsing boundaries (Cisek et al. 2009; Chandrasekaran and Hawkins 2019; Ditterich 2006; Hawkins et al. 2015).”

“Time-varying weights have been shown to better predict animals’ choice in certain tasks [46], and psychophysical kernels are sometimes skewed towards one end of the trial[47,48], suggesting that decoding could also be suboptimal in time.”

“…cortex (Gold and Shadlen, 2001; Shadlen and Newsome, 2001; Roitman and Shadlen, 2002; Yang and Shadlen, 2007; Kiani et al., 2008; Meister et al., 2013; Park et al., 2014; de Lafuente et al., 2015; Shadlen et al., 2016) and the frontal eye fields (Gold and Shadlen, 2000, 2003; Ding and Gold, 2012).”

“Finally, a recent elegant study on the formation of motor intentions for reaches versus saccades in MIP and LIP (de Lafuente et al. 2015) has shown that the gradual accumulation of information about decision signals in the activity of neurons in MIP leads to the formation motor intentions for a…”

“The median latencies for PMd were significantly shorter than for M1 (Wilcoxon rank sum test, p 0.001) and were similar to other reports of decision-related signals in PMd (Thura and Cisek, 2014, Chandrasekaran et al., 2017) and MIP (de Lafuente et al., 2015).”

“…these sites is consistent with a process of evidence accumulation, building gradually over time at a rate that is proportional to the strength of the sensory information, reaching a fixed threshold just before a response is made, and reliably predicting the animal’s choice and response time 1–6 .”

“The lateral PFC, LIP and MIP are important processing stages for mediating decision-making tasks (de Lafuente et al., 2015; Ding and Gold, 2012; Gold and Shadlen, 2007; Huk et al., 2017; Kim and Shadlen, 1999; Padoa-Schioppa and Assad, 2006; Platt and Glimcher, 1999; Rossi-Pool et al., 2017;…”

“In another brain area it might represent a plan to do something else, such as reach [9, 19] or implement a rule [20], perhaps.”

“A variety of neuroimaging studies have already demonstrated their roles in decision making (Heekeren et al., 2004, 2008; Philiastides and Sajda, 2007; Ruff et al., 2010; de Lafuente et al., 2015; Lamichhane et al., 2016).”

“…have been confirmed in a simple but well-controlled perceptual task that by now has become the classical model of decision-making: the saccadic decisions made by appropriately trained monkeys (e.g. Palmer et al., 2005; Shadlen and Kiani, 2013; Kiani et al., 2014; de Lafuente et al., 2015).”

“This supports a notion that choice-related signals in LIP are partially saccade-specific and partially general, whereas PRR signals are more strongly embodied (de Lafuente et al. 2015; Kubanek, Li, et al. 2015).”

“39 To account for these high-level roles, it has been proposed that LIP forms a ‘‘priority map’’ of space, identifying important spatial locations and then propagating that information to other areas, including PRR, to further cognitive or motor goals (Figure 1A, spatial hub or priority map model).”

“Similar encoding of the DV has been found in many other brain structures (de Lafuente et al. 2015; Deverett et al. 2018; Ding and Gold 2010, 2012; Donner et al. 2009; Horwitz and Newsome 1999; Kiani et al. 2014b; Kim and Basso 2008; Kim and Shadlen 1999; Peixoto et al. 2018; Ratcliff et al. 2003)…”

“© 2017 Federation of European Neuroscience Societies and John Wiley & Sons Ltd [e.g. lateral (LIP) or medial (MI) intraparietal areas (de Lafuente et al., 2015)] are thought to play a pivotal role by influencing perceptual decisions at two levels.”

“…perceptual decisions in static environments have identi fi ed two human neurophysiological signals that evolve with similar integration dynamics, with one - the centroparietal positivity - appearing to compute the running integral and continuously feed it to the other - motor beta lateralisation.”

“A mixed effect analysis showed a main effect of Cue Condition on alpha amplitude (F(1,52527) = 10.10, p = 0.001), such that there was significantly greater alpha desynchronisation in the neutral cue condition, consistent with increased task engagement in this condition.”

“(7) with a fi nite bin size have similar limitations 31,47 (Methods), although accurate estimation is possible using large bin sizes 48 .”