Neural dynamics of choice: Single-trial analysis of decision-related activity in parietal cortex

“Decision-related activity has been observed in a variety of brain areas, including the lateral intraparietal area (LIP) in parietal cortex (Shadlen and Newsome, 2001; Roitman and Shadlen, 2002; Churchland et al., 2008), areas in (pre)frontal cortex (Kim and Shadlen, 1999), and the superior colliculus (SC; Horwitz and…”

“In contrast, Roitman and Shadlen (2002) and Churchland et al. (2011) have provided indirect arguments for LIP neurons undergoing a gradual firing rate change.”

“This is convenient because it allows the mechanism to extend to decisions among more than two options (Bollimunta et al., 2012; Churchland et al., 2008; Ditterich, 2010; Usher and McClelland, 2001).”

“In Macaca mulatta, the firing rates of some neurons seem to behave like processes from diffusion models (Bollimunta et al., 2012; Ding and Gold, 2010, 2012a; Hanes and Schall, 1996; Heitz and Schall, 2012; Kiani and Shadlen, 2009; Pouget et al., 2011; Purcell et al., 2010; Purcell et al., 2012;…”

“We focus on LIP because numerous studies suggest that neurons in this area exhibit the signatures of both evidence accumulation and a decision bound that leads to commitment for saccadic decisions (Shadlen and Newsome, 2001; Roitman and Shadlen, 2002; Hanks et al., 2006; Yang and Shadlen, 2007; Churchland et al., 2008…”

“[28]) has uncovered similar firing rate patterns in multiple brain regions, most prominently in the frontal eye fields (FEF) [4,29,30,31!!], but also in other regions (dorsolateral prefrontal cortex [29]; superior colliculus [32–34]; and striatum [35]; Figure 1c).”

“Past studies have documented cortical and subcortical fluctuations in neural activity that might correspond to changes of mind [7, 29, 38].”

“While changes of mind have been hypothesized to occur during decision making, and have even been observed when sensory evidence changes (Horwitz and Newsome, 2001; Bollimunta et al., 2012; Kiani et al., 2014; Thura and Cisek, 2014), little has been known about how decisions proceed during truly free choices.”

“Although such studies have characterized how external sensory information is represented and interpreted by the brain to influence behavior (Bogacz et al., 2010; Bollimunta et al., 2012; Gold and Shadlen, 2007; Hanks et al., 2014; Heekeren et al., 2008; Nienborg and Cumming, 2009), the neural computations that support…”

“On the other hand, the lateralized readiness potential might be useful to observe and investigate “changes of mind” (Albantakis et al., 2012; Bollimunta et al., 2012; Resulaj et al., 2009) during the ongoing decision.”

“There have been many studies that also show decision-making processes in parietal cortex (Bollimunta et al. 2012; Platt and Glimcher 1999; Shadlen and Newsome 2001), prefrontal cortex (Bechara et al. 1999; Hoshi et al. 1999; Rainer et al. 1998), orbitofrontal cortex (Padoa-Schioppa and Assad 2006;…”

“…et al., 2010; Rolls et al., 2010; Deco et al., 2013), as well as bistable perception (Deco et al., 2007; Moreno-Bote et al., 2007), “changes of mind” (Bollimunta et al., 2012), and Bayesian inference through sampling (Moreno-Bote et al., 2007, 2011), and have been shown to outperform perfect…”

“However, an alternative analysis of the latter task revealed ramping as the typical dynamics during stimulus acquisition, with rapid transitions corresponding only to changes of mind [81].”

“Such ‘firing rate-state’ models have been successful in modeling both choice related hidden variables and the dynamics of perceptual processes (Seidemann et al., 1996, Jones et al., 2007, Kemere et al., 2008, Bollimunta et al., 2012, Deco et al., 2013, Moran and Katz, 2014).”

“2012) or combinations of jumps and ramps (Bollimunta et al. 2012).”

“We also could extend the stepping model to a general hidden Markov model, allowing for more than three discrete firing rates, with more flexible transition dynamics that allow for more than one transition per trial (Bollimunta et al., 2012).”

“The neural representation of the decision variable remains unknown since its unique trajectories on single trials are not observable 10,11 , and decision-related responses of cortical neurons are complex and heterogeneous 15,21,22 .”

“The richness of saccadic planning is particularly evident in perceptual decision-making tasks, where the neuronal activity continually tracks the current state of the evidence for choosing the target in the neuron’s RF (Mazurek et al., 2003; Bollimunta et al., 2012).”

“Such experiments are just starting to be reported (Bollimunta et al., 2012), and more results from this enterprise are eagerly anticipated.”

“Recent years have seen burgeoning interest in applying model selection in neuroscience, both for the firing patterns of single neurons (Bollimunta et al., 2012; Latimer et al., 2015b,a, 2016, 2017; Rossant et al., 2011), as well as for functional imaging and encephalographic signals (Durstewitz et…”

“Starting from a spike count for each cell and each trial (2-ms bins) aligned all at the same event, in order to generate an emission sequence, we assigned one symbol to each bin (Bollimunta et al., 2012; Mazurek et al., 2018).”

“…a small but growing body of literature that leverages simultaneous electrophysiological population recordings to explore the neural substrate of internal cognitive phenomena at the level of single trials (Bollimunta et al., 2012, Kaufman et al., 2015, Kiani et al., 2014b, Rich and Wallis, 2016).”

“…Gold and Shadlen, 2007; Ratcliff et al., 2016; Shinn et al., 2020; Wiecki et al., 2013; Zylberberg et al., 2016) or neural response data (e.g., Bollimunta et al., 2012; Brody and Hanks, 2016; Churchland et al., 2011; Ditterich, 2006; Genkin et al., 2021; Hanks et al., 2015; Howard et al.,…”

“Evidence of covert subthreshold mental vacillations has been reported in neurophysiological studies (Bollimunta et al. 2012; Kiani et al. 2014).”

“Specifically, we used the mathematical model of Kiani et al. (2008) to estimate the amount of motion energy that would be coded by MT neurons in the true motion direction, in the opposite direction, and in the two orthogonal directions (see also Bollimunta et al., 2012).”

“One approach to address this question is to formulate models of decision-making behavior as generative models of neural activity (Dit-terich, 2006; Bollimunta et al., 2012; Latimer et al., 2015; Zoltowski et al., 2019).”

“Finally, we describe our observations of spiking irregularity in several cortical areas,whichrevealsystematicdifferencesfromsensorytomotorareas and indicate that Poisson irregularity is a rare exception, not a rule.”

“The hypothetical signal that is posited to stop accumulation on the observed neuron’s Tout trials has never been identified in these experiments, nor have the “winning” and “losing” accumulator responses been simultaneously measured and directly tied into this model, although such datasets are now possible to acquire…”

“, 2015), and the streak index (SI) (Horwitz and Newsome, 2001; Bollimunta et al., 2012).”

“…decision-making tasks, and activity in these neurons has been related to continuously-graded integration of sensory evidence (e.g., Shadlen and Newsome, 2001; Bollimunta et al., 2012; see Gold and Shadlen, 2007) as well as the degree of confidence in perceptual decisions (Kiani and Shadlen, 2009).”

“Classic frequentist HMMs applied to neural data have used a univariate multinomial distribution for emission probabilities (Bollimunta et al., 2012; Mazurek et al., 2018; Diomedi et al., 2021), encoding which of N neurons is spiking in each time bin, and choosing a random neuron if multiple neurons spike in the same b…”

“Recently, [36] reliable evidence has been provided for the hypothesis that LIP neurons display a gradual ramp.”

“These results somewhat justify the use of a small number of initial guesses seen in previous works, sometimes as small as 5 or 10 [12,13,15,17,32,35].”

“The neural representation of the decision variable remains unknown as its unique trajectories on single trials are not observable 3,4 , and decision-related responses of cortical neurons are complex and heterogeneous 8,11,20 .”

“In particular, attractor dynamics, in which the network state moves towards discrete [9, 16] or along continuous [8, 17] attractor states, have been studied extensively as a potential neural mechanism for decision-making and evidence accumulation [18, 19].”

“For RT trials integration activity is assumed to begin from 200 ms after stimulus onset and terminates 50 ms before saccade initiation, following (Bollimunta et al., 2012), where we use target acquisition time as a proxy for saccade initiation.”

“Several recent studies have recovered single-trial dynamical information in structures close to motor output, based upon neuronal spiking data (Thura and Cisek, 2014; Kaufman et al., 2015; Murakami et al., 2014; Bollimunta et al., 2012; Kiani et al., 2014; Carnevale et al., 2015).”

“They can explain the 50 distribution of choices and associated response times (RTs) for a wide range of decision tasks (Ratcliff 51 and Smith, 2004) and are consistent with decision-related neural activity, both averaged across trials as 52 well as on a single-trial level (Ditterich, 2006; Bollimunta et al., 2012).”

“When monkeys perform a random-dot motion direction discrimination task and report the choice with a goal-directed eye movement, the activity of neurons in the lateral intraparietal area (LIP) in parietal cortex reflects the ongoing decision [1, 18, 19] and has even been shown to have a causal effect on the outcome of…”

“One recent study focused on model comparison for spike trains recorded in macaque lateral intraparietal cortex (LIP), a putative decision-making area (Bollimunta, Totten & Ditterich 2012).”

“Streak index analysis (52, 53) also supports this interpretation.”

“Streak index analysis 50,51 also supports this interpretation.”

“To overcome this limitation in an unsupervised manner, methods like Hidden Markov Models 19,70–73 offer a powerful alternative by segmenting neural time series into distinct temporal states.”

“…during the trial made the line attractor model, which requires the network state to stay close to attractor states ( Inagaki et al., 2019 ; Luo et al., 2023 ; Seung, 1996 ; Bollimunta et al., 2012 ), inadequate for explaining the neural activity encoding evidence accumulation in reversal learning.”

“…sequence of units (Baeg et al., 2003; Fujisawa et al., 2008; Harvey et al., 2012; Morcos & Harvey, 2016; Rajan et al., 2016), sequence of patterns (Bollimunta et al., 2012; Goldman, 2009; Wehr & Laurent, 1996), and combinations thereof (M. M. Churchland et al., 2012; Kaufman, Churchland, Ryu, &…”

“A strong research focus lies on the lateral intraparietal area (LIP) of the macaque monkey (Shadlen and Newsome, 2001; Roitman and Shadlen, 2002; Hanks et al., 2006; Churchland et al., 2008; Kiani and Shadlen, 2009; Bollimunta et al., 2012), but as pointed out above, current evidence is not conclusive regarding the ge…”