Special Issue “Attention & Motor Processes”: Research ReportDistinct saccade planning and endogenous visuospatial attention maps in parietal cortex: A basis for functional differences in sensory and motor attention
Introduction
A skilled magician will get the audience to attend to one aspect of the performance so spectators will miss the sleight of hand. It doesn't take much; a sudden movement in a person's peripheral vision or instruction to carefully watch a particular activity is enough to cause the audience to move their eyes elsewhere. These magic tricks require shifts of visual attention with and without concomitant eye movements. This observation illustrates the longstanding debate regarding the level of connectedness between the neural mechanisms underlying visuospatial attention and eye movements. If one can attend to a location without moving the eyes or plan to move the eyes in one direction while attending to another, are endogenous covert visual and saccade planning attentional mechanisms separate?
While activity in topographically organized regions, or maps, of parietal cortex contribute to both endogenous visuospatial attention (Brefczynski & DeYoe, 1999; Silver, Ress, & Heeger, 2005; Szczepanski, Pinsk, Douglas, Kastner, & Saalmann, 2013) and saccade planning (Schluppeck, Curtis, Glimcher, & Heeger, 2006; Sereno, Pitzalis, & Martinez, 2001), continued controversy exists regarding the role of this brain region (See Freedman and Ibos (2018) for a thorough examination of the ongoing debate) in the necessary selection and integration of both visual and motor information to successfully execute goal-directed movements (Gold & Shadlen, 2000). Parietal cortex activity has previously been labeled as primarily involved in the sensory aspects of a task (Bisley & Goldberg, 2010), or only in the context of the upcoming movement (Quian Quiroga, Snyder, Batista, Cui, & Andersen, 2006), or both (Freedman & Ibos, 2018). Complicating this issue, evidence from non-human primates suggests that neurons in portions of parietal cortex demonstrate different coding mechanisms in the same population of neurons for sensory and motor components, depending on task demands (Bennur & Gold, 2011).
Consistent with the notion that the same regions of parietal cortex contribute to both the sensory and motor components of a task, some have hypothesized that spatial attention is a singular neurophysiological process across modalities involving the same set of neurons via a salience map (Bisley & Goldberg, 2003; Purcell, Schall, Logan, & Palmeri, 2012). Evidence in support of this theory includes the significant overlap of visual attention and saccade planning-related activation in humans (Astafiev et al., 2003), and an improvement in attention-mediated behavioral performance when visual and motor targets overlap (Abrams, Oonk, & Pratt, 1998; Carbone & Schneider, 2010; Macaluso, Driver, & Frith, 2003). However, we and others have demonstrated that endogenous covert visual attention and saccade planning, and/or their associated regions of activation in posterior parietal cortex, can be dissociated (Casteau & Smith, 2020; Hu, Bu, Song, Zhen, & Liu, 2009; Khan et al., 2009; Konen, Kleiser, Bremmer, & Seitz, 2007; Puckett, Bollmann, Barth, & Cunnington, 2017; Quian Quiroga et al., 2006; Snyder, Batista, & Andersen, 1998), with attention-mediated task performance primarily being influenced by changes in domain-specific visual or motor task demands (Huddleston et al., 2013).
A tangle of meso-scale human functional neuroimaging studies performed at the group level and using different experimental approaches add to this debate regarding the organization of attention maps in parietal cortex. Evaluating group-level activation data in the same participants for both endogenous visual attention and saccade planning activation, but not actual topography, leads to significant overlap across tasks within parietal cortex (Astafiev et al., 2003; Corbetta et al., 1998). This group level analysis may obliterate any individual variation in parietal cortex organization, a brain region known for dynamic organization (Corbetta, Miezin, Dobmeyer, Shulman, & Petersen, 1990; Greenberg, Esterman, Wilson, Serences, & Yantis, 2010; Li, Ostwald, Giese, & Kourtzi, 2007) and greater variability among participants (Frost & Goebel, 2012; Scolari, Seidl-Rathkopf, & Kastner, 2015). Individual differences, measured by extent of activation or functional magnetic resonance imaging (fMRI) Blood Oxygen Level Dependent (BOLD) signal quality, in topographic maps correlate with behavioral performance on a number of tasks including endogenous covert visuospatial attention (Huddleston & DeYoe, 2008; Szczepanski, Konen, & Kastner, 2010), working memory (Hampson, Driesen, Skudlarski, Gore, & Constable, 2006), and delayed saccades (Kunowski & Huddleston, 2011). Thus, individual differences must be recognized when comparing cortical patterns of activation during both saccade planning and endogenous covert visual attention tasks in this particular brain region.
In addition to group level analysis challenges, different paradigms have been used to study saccade planning. A potential confound of previous saccade planning topography studies is the rapid onsets of peripheral visual targets, which may induce a spatially-specific response co-localizing the focus of saccade planning and involuntary capture of visuospatial attention. This stimulus feature may influence the overall allocation of attention during the task (Hopfinger & West, 2006). Evaluating visual attention and saccade planning through mapping of pro- and anti-saccades addresses this issue by spatially separating the visual stimulus and the movement target. However, these actions also require an inhibition of a pro-saccade to the visual target, creating increased cortical activation (Connolly, Goodale, Desouza, Menon, & Vilis, 2000; D'eSouza, Menon, & Everling, 2002) and potentially compromising any interpretation of activation patterns. Additionally, mapping of anti-saccades has been limited to left/right hemifields at the group level (Medendorp, Goltz, & Vilis, 2005), limiting the ability to address potential topography. To address these methodological concerns, we developed a saccade planning task in which the central focus of visual attention did not have a spatial component during saccade planning, allowing us to isolate the spatially-specific saccade planning signal in parietal cortex.
To our knowledge, the spatial selectivity of saccade planning and endogenous visual attention maps across multiple targets within each hemisphere and within participants has not been previously reported. We specifically addressed two components of these maps including spatial specificity and individual variability. The overall objective of the current study was to resolve the extent to which saccade planning and endogenous covert visual attention maps exist in the same geographical regions of parietal cortex as a first step to determine if a single spatial saliency map exists in humans versus the presence of separate maps. Secondarily, we quantified the level of spatially-specific congruency in regions of map overlap as a possible location for information transfer from sensory to motor aspects of the task. We hypothesized that cortical activation occurs in different parietal regions based on task demands. We further hypothesized that the organization of these parietal maps would vary among individuals due to the variability in the organization of parietal cortex (Frost & Goebel, 2012), and the flexibility of this area to encode task-specific parameters (Harvey, Klein, Petridou, & Dumoulin, 2013).
Section snippets
Methods
No part of the study procedures or analyses was pre-registered prior to conducting the research. We report how we determined our sample size, all data exclusions (if any), all inclusion/exclusion criteria, all manipulations, and all measures in the study. All inclusion and exclusion criteria were established prior to the start of the study. All fMRI analyses were performed using publicly available AFNI software (R.W. Cox, 1996). Raw functional neuroimaging data (.AFNI BRIK and HEAD files) for
Results
Consistent with previous studies (Leone, Toni, & Medendorp, 2014; Schluppeck et al., 2006; Sereno et al., 2001), we identified regions of parietal cortex responsive to spatial shifts in saccade planning (Fig. 2). Importantly, this representation occurred while visual attention was maintained in the center of the screen due to the task requirement to monitor the central RSVP for task cues and with no peripheral transients to potentially involuntarily capture visual attention. This spatially
Discussion
The concept of ‘motor attention’ has several definitions including decision making through attentional selection among motor plans (Goldberg & Segraves, 1987; Toni, Thoenissen, & Zilles, 2001), selecting an action (Pashler, 1991), covert planning of movement (Rushworth, Nixon, Renowden, Wade, & Passingham, 1997, Rushworth, Paus, & Sipila, 2001), preparing and maintaining a motor plan (Symes, Ottoboni, Tucker, Ellis, & Tessari, 2010), and attending to predicted proprioceptive sensations for
Conclusions
Saccade planning has many components, and we consider motor attention (aka motor intention) to be one of the critical processes in that planning. Based on our current findings, and those of others, we posit that similarities exist in the potential mechanisms of the selection of salient spatial information across endogenous covert visual attention and movement planning (in this case, saccades). However, the processes, or at least the maps on which they act, are dissociable and in fact separate.
Open practices
The study in this article earned Open Materials and Open Data badges for transparent practices. Materials and data for the study are available at https://dc.uwm.edu/kinesiology_facdata/1/.
Funding
This work was supported by the National Center for Advancing Translational Sciences, National Institutes of Health, UL1TR001436. The sponsor had no involvement in this study or manuscript.
Author contributions
Wendy Huddleston: Conceptualization, Methodology, Formal analysis, Writing – original draft, Visualization, Validation, Supervision, Project administration, Funding acquisition. Alex Swanson: Investigation, Data curation, Visualization, Writing – review and editing. James Lytle: Investigation, Writing – review and editing. Michael Aleksandrowicz: Investigation, Validation, Writing – review and editing.
Declaration of competing interest
The authors declare no competing interests.
Acknowledgments
We would like to acknowledge Matt Verber for his assistance with programming the stimulus.
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2021, Trends in NeurosciencesCitation Excerpt :Likewise, in humans, the early laterality of visual evoked event-related potentials (ERPs) correlates with covert but not presaccadic attention [114], and transcranial magnetic stimulation (TMS) over FEF has revealed a clear temporal dissociation of saccade preparation and attention [115]. These results are consistent with the findings that saccade preparation and covert attention – despite involving overlapping neural regions – are neurophysiologically distinct phenomena [109,116]. In summary, neurophysiological evidence reveals that distinct neural populations in FEF and SC control covert attention and saccade preparation in human and non-human primates, potentially giving rise to differences in their perceptual correlates.