Effect of parietal lobe lesions on saccade targeting and spatial memory in a naturalistic visual search task

The eye movements of two patients with parietal lobe lesions and four normal observers were measured while they performed a visual search task with naturalistic objects. Patients were slower to perform the task than the normal observers, and the patients had more fixations per trial, longer latencies for the first saccade during the visual search, and less accurate first and second saccades to the target locations during the visual search. The increases in response times for the patients compared to the normal observers were best predicted by increases in the number of fixations. In order to investigate the effects of spatial memory on search performance, in some trials observers saw a preview of the search display. The patients appeared to have difficulty using previously viewed information, unlike normal observers who benefit from the preview. This suggests a spatial memory deficit. The patients' deficits are consistent with the hypothesis that the parietal cortex has a role in the selection of targets for saccades, in memory for target location.     

Low-Level Visual Information Is Maintained across Saccades,Allowing for a Postsaccadic Handoff between Visual Areas

Experience seems continuous and detailed despite saccadic eye movements changing retinal input several times per second. There is debate whether neural signals related to updating across saccades contain information about stimulus features, or only location pointers without visual details. We investigated the time course of low-level visual information processing across saccades by decoding the spatial frequency of a stationary stimulus that changed from one visual hemifield to the other because of a horizontal saccadic eye movement. We recorded magnetoencephalography while human subjects (both sexes) monitored the orientation of a grating stimulus, making spatial frequency task irrelevant. Separate trials, in which subjects maintained fixation, were used to train a classifier, whose performance was then tested on saccade trials. Decoding performance showed that spatial frequency information of the presaccadic stimulus remained present for ∼200 ms after the saccade, transcending retinotopic specificity. Postsaccadic information ramped up rapidly after saccade offset. There was an overlap of over 100 ms during which decoding was significant from both presaccadic and postsaccadic processing areas. This suggests that the apparent richness of perception across saccades may be supported by the continuous availability of low-level information with a “soft handoff” of information during the initial processing sweep of the new fixation.SIGNIFICANCE STATEMENT Saccades create frequent discontinuities in visual input, yet perception appears stable and continuous. How is this discontinuous input processed resulting in visual stability? Previous studies have focused on presaccadic remapping. Here we examined the time course of processing of low-level visual information (spatial frequency) across saccades with magnetoencephalography. The results suggest that spatial frequency information is not predictively remapped but also is not discarded. Instead, they suggest a soft handoff over time between different visual areas, making this information continuously available across the saccade. Information about the presaccadic stimulus remains available, while the information about the postsaccadic stimulus has also become available. The simultaneous availability of both the presaccadic and postsaccadic information could enable rich and continuous perception across saccades.     

Maintenance of visual stability in the human posterior parietal cortex

Visual stability refers to our stable visuospatial perceptions despite the unstable visual input caused by saccades. Functional neuroimaging results, studies on patients with posterior parietal cortex (PPC) lesions, and single-unit recordings in the lateral intraparietal sulcus of primates indirectly suggest that the PPC might be a potential locus of visual stability through its involvement with spatial remapping. Here we directly explored the role of the PPC in visual stability by applying transcranial magnetic stimulation (TMS) while participants performed a perisaccadic displacement detection task. We show that TMS over the PPC but not a frontal control site alters sensitivity to displacement detection when administered just before contralateral saccades and that a general impairment in attention or in the perception of apparent motion cannot account for the decreased sensitivity. The specific relationship between the timing of TMS and saccade direction demonstrates that saccadic suppression of displacement (SSD) is likely a consequence of noisy contralateral spatial representations in the PPC around the time of a saccade. The same mechanism may keep the unstable visual world in the temporal proximity of saccades from reaching our consciousness.     

Oculomotor functions of the parietal lobe: Effects of chronic lesions in humans

This review summarises research in patients with chronic lesions of parietal oculomotor cortex and compares their oculomotor performance to patients with lesions of the frontal eye field (FEF). The observations identify the oculomotor functions for which these regions are indispensable, and explore dynamic interactions within cortical and subcortical networks for oculomotor control. The experiments examined endogenously generated saccades, saccades to visual targets, antisaccades, saccade choice and saccade remapping for inhibitory spatial tagging. The findings suggest that the key function of parietal oculomotor cortex is the computation of sensorimotor transformations, rather than the initiation of either voluntary or reflexive saccades. They also reveal the re-organisation of cortico-subcortical networks after brain injury, and provide insight into their dynamic interactions: FEF lesions result in disinhibition of reflexive saccades toward the contralesional field and an impairment of reflexive saccades toward the ipsilesional field; whereas parietal lesion result in the opposite pattern.     

Neuronal substrate of the saccadic inhibition deficit in schizophrenia investigated with 3-dimensional event-related functional magnetic resonance imaging

BACKGROUND: Several studies have shown that the ability to suppress automatic saccadic eye movements is impaired in patients with schizophrenia as well as in their first-degree relatives, and suggest that this impairment is a potential vulnerability marker for schizophrenia. The neurobiological mechanisms underlying normal saccade production and inhibition, revealed in primate studies, indicate that the impairment may result from a failure of the oculomotor system to effectively exert inhibitory control over brainstem structures. Functional localization of the affected brain structure(s) potentially provides a physiological measure for the investigation of vulnerability markers in schizophrenia. METHODS: The hemodynamic response to discrete visual stimuli was measured during prosaccades (saccades toward a peripheral stimulus), antisaccades (saccades toward a position opposite to a peripheral stimulus), and active fixation (holding fixation and ignoring a peripheral stimulus) in 16 patients with schizophrenia receiving atypical neuroleptics and 17 healthy control subjects using an event-related functional magnetic resonance imaging task design. RESULTS: Brain responses were detected in the frontal and parietal regions of the oculomotor system in all 3 tasks. Patients made more errors during inhibition tasks and exhibited a selective failure to activate the striatum during the inhibition of saccades. In other regions that were active during inhibition, specifically the supplementary and frontal eye fields, no difference was found between patients and control subjects. CONCLUSIONS: A frontostriatal network is engaged in the suppression of automatic eye movements. The results indicate that abnormalities in this network, rather than the selective dysfunction of prefrontal brain regions, underlie the saccade inhibition deficit in schizophrenia.     

Deficits in saccadic eye-movement control in Parkinson's disease

In contrast to their slowed limb movements, individuals with Parkinson's disease (PD) produce rapid automatic eye movements to sensory stimuli and show an impaired ability to generate voluntary eye movements in cognitive tasks. Eighteen PD patients and 18 matched control volunteers were instructed to look either toward (pro-saccade) or away from (anti-saccade) a peripheral stimulus as soon as it appeared (immediate, gap and overlap conditions) or after a variable delay; or, they made sequential saccades to remembered targets after a variable delay. We found that PD patients made more express saccades (correct saccades in the latency range of 90-140 ms) in the immediate pro-saccade task, more direction errors (automatic pro-saccades) in the immediate anti-saccade task, and were less able to inhibit saccades during the delay period in all delay tasks. PD patients also made more directional and end-point errors in the memory-guided sequential task. Their inability to plan eye movements to remembered target locations suggests that PD patients have a deficit in spatial working memory which, along with their deficit in automatic saccade suppression, is consistent with a disorder of the prefrontal-basal ganglia circuit. Impairment of this pathway may release the automatic saccade system from top-down inhibition and produce deficits in volitional saccade control. Parallel findings across various motor, cognitive and oculomotor tasks suggest a common mechanism underlying a general deficit in automatic response suppression.     

Oculomotor evidence for neocortical systems but not cerebellar dysfunction in autism

OBJECTIVE: To investigate the functional integrity of cerebellar and frontal systems in autism using oculomotor paradigms. BACKGROUND: Cerebellar and neocortical systems models of autism have been proposed. Courchesne and colleagues have argued that cognitive deficits such as shifting attention disturbances result from dysfunction of vermal lobules VI and VII. Such a vermal deficit should be associated with dysmetric saccadic eye movements because of the major role these areas play in guiding the motor precision of saccades. In contrast, neocortical models of autism predict intact saccade metrics, but impairments on tasks requiring the higher cognitive control of saccades. METHODS: A total of 26 rigorously diagnosed nonmentally retarded autistic subjects and 26 matched healthy control subjects were assessed with a visually guided saccade task and two volitional saccade tasks, the oculomotor delayed-response task and the antisaccade task. RESULTS: Metrics and dynamics of the visually guided saccades were normal in autistic subjects, documenting the absence of disturbances in cerebellar vermal lobules VI and VII and in automatic shifts of visual attention. Deficits were demonstrated on both volitional saccade tasks, indicating dysfunction in the circuitry of prefrontal cortex and its connections with the parietal cortex, and associated cognitive impairments in spatial working memory and in the ability to voluntarily suppress context-inappropriate responses. CONCLUSIONS: These findings demonstrate intrinsic neocortical, not cerebellar, dysfunction in autism, and parallel deficits in higher order cognitive mechanisms and not in elementary attentional and sensorimotor systems in autism.     

Cortical control of double-step saccades: Implications for spatial orientation

To accurately localize a visual target in space despite eye movement-induced shifts of its retinal image, the brain must take into account both its retinal location and information about current eye position or at least the preceding eye displacement. We examined this ability with respect to saccadic eye movements by applying “double-step” stimuli, where the locations of two sequentially flashed target lights have to be fixated by two successive saccades performed after their disappearance. As the 2nd saccade will not start at the spatial location from which the 2nd target was seen, a dissonance arises between its retinal coordinates and the motor coordinates of the required 2nd saccade. Nevertheless, these saccades were performed quite accurately by 32 healthy human adults. To investigate the contribution of the cerebral cortex, we recorded horizontal double-step saccades in 35 patients with focal unilateral hemispheric lesions. Whereas frontal lesions impaired temporal properties, posterior parietal lesions caused spatial dysmetria or failure of even ipsiversive 2nd saccades following contraversive 1st saccades. This reflects an inability to compensate for retino-spatial dissonance by using nonretinal information (corollary discharge) about eye displacement associated with a previous saccade into the contralesional hemifield. In conclusion, the parietal cortex is crucial for spatial constancy across saccades.     

Vestibular integration in human cerebral cortex contributes to spatial remapping

The process of visuo-spatial updating is crucial in guiding human behaviour. While the parietal cortex has long been considered a principal candidate for performing spatial transformations, the exact underlying mechanisms are still unclear. In this study, we investigated in a patient with a right occipito-parietal lesion the ability to update the visual space during vestibularly guided saccades. To quantify the possible deficits in visual and vestibular memory processes, we studied the subject's performance in two separate memory tasks, visual (VIS) and vestibular (VES). In the VIS task, a saccade was elicited from a central fixation point to the location of a visual memorized target and in the VEST task, the saccade was elicited after whole-body rotation to the starting position thus compensating for the rotation. Finally, in an updating task (UPD), the subject had to memorize the position of a visual target then after a whole-body rotation he had to produce a saccade to the remembered visual target location in space. Our main findings was a significant hypometria in the final eye position of both VEST and UPD saccades induced during rotation to the left (contralesional) hemispace as compared to saccades induced after right (ipsilesional) rotation. Moreover, these deficits in vestibularly guided saccades correlated with deficits in vestibulo-ocular time constant, reflecting disorders in the inertial vestibular integration path. We conclude that the occipito-parietal cortex in man can provide a first stage in visuo-spatial remapping by encoding inertial head position signals during gaze orientation.     

Characterization of oculomotor and visual activities in the primate pedunculopontine tegmental nucleus during visually guided saccade tasks

The pedunculopontine tegmental nucleus (PPTN) has anatomical connections with numerous visuomotor areas including the basal ganglia, thalamus, superior colliculus and frontal eye field. Although many anatomical and physiological studies suggest a role for the PPTN in the control of conditioned behavior and associative learning, the detailed characteristics of saccade‐ and visual‐related activities of PPTN neurons remain unclear. We recorded the activity of PPTN neurons in monkeys (Macaca fuscata ) during visually guided saccade tasks, and examined the response properties of saccade‐ and visual‐related activities such as time course, direction selectivity and contextual modulation. Saccade‐related activity occurred either during saccade execution or after saccade end. The preferred directions of the neuronal activity were biased toward the contralateral and upward sides. Half of the saccade‐related neurons showed activity modulation only for task saccades and not for spontaneous saccades outside the task. Visually‐responsive neurons responded with short latencies. Some responded to the appearance of the visual stimulus in a directionally selective manner, and others responded to both the appearance and disappearance of the visual stimulus in a directionally non‐selective manner. Many of these neurons exhibited distinct visual responses to the appearance of two different stimuli presented under different stages of the task, whereas a population of the neurons responded equally to the disappearance of the two stimuli. Thus, many PPTN neurons exhibited context‐dependent activity related to the visuomotor events, consistent with a role in controlling conditioned behavior.     

Do parietal cortical lesions impair spatial attention or allocentric spatial perception?

It remains unclear whether monkeys with large parietal cortical lesions fail "landmark" tasks because they cannot judge the relative distances between landmark and response locations, or because they fail to attend to, or even to notice, the landmark. Monkeys with small posterior parietal (SPP), large posterior parietal (LPP), superior temporal sulcus (STS), or frontal eye field (FEF) lesions were tested on a landmark task in which the physical salience of the landmark and its location varied. Only the LPP monkeys were impaired, seemingly because they overtly failed to shift attention during each trial, responding to whichever food well they looked at first. A task based on one used with neurological patients was therefore introduced in which the monkeys had to discriminate between two white square plaques each containing a spot, where the spot on the positive stimulus was centrally placed. Solving this task requires an allocentric judgement about the relative location of each spot to the edges of the plaque. Even on the most difficult discrimination, monkeys with large parietal lobe lesions were unimpaired. The deficits previously reported on landmark tasks probably reflect a failure of spatial attention or attention to objects rather than an inability to judge allocentric spatial relationships.     

Time course of cross-hemispheric spatial updating in the human parietal cortex

In human parietal cortex, the retinal location of a just seen visual stimulus is updated from one hemisphere to the other, when a horizontal eye movement brings the representation of the stimulus into the opposite visual hemifield. The present study aimed to elucidate the time course of this process. Twelve subjects performed an updating task, in which a filled circle was shown before a horizontal saccade, requiring updating of stimulus location, and a control task without visual stimulation before the saccade. Electroencephalogram (EEG) and electrooculogram (EOG) were recorded while subjects performed the tasks and LORETA source analysis was performed on event-related potential (ERP) components. ERP amplitudes were more positive in the updating condition in comparison to the control condition in two latency windows. An early positive wave starting at about 50 ms after saccade offset and originating in the posterior parietal cortex contralateral to saccade direction probably reflects the integration of saccade-related and visual information and thus the updating process. A shift of the representation of the to-be-updated stimulus to the opposite hemisphere is reflected in a later component starting approximately 400 ms after saccade offset, which is related to memory and originates in the PPC ipsilateral to saccade direction and thus contralateral to the spatial location of the updated visual stimulus.     

Post-saccadic updating of visual space in the posterior parietal cortex in humans

Updating of visual space takes place in the posterior parietal cortex to guarantee spatial constancy across eye movements. However, the timing of updating with respect to saccadic eye movements remains a matter of debate. In the present study, event-related potentials (ERPs) were recorded in 15 volunteers during a saccadic double-step task to elucidate the time course of the updating process. In the experimental condition updating of visual space was required, because both saccade targets had already disappeared before the first saccade was executed. A similar task without updating requirements served as control condition. ERP analysis revealed a significantly larger slow positive wave in the retino-spatial dissonance condition compared to the control condition, starting between 150 and 200 ms after first saccade onset. Source analysis showed an asymmetry with respect to the direction of the first saccade. Whereas the source was restricted to the right PPC in trials with leftward first saccades, left and right PPC were involved in rightward trials. The results of the present study suggest that updating of visual space in a saccadic double-step task occurs not earlier than 150 ms after the onset of the first saccade. We conclude that extraretinal information about the first saccade is integrated with motor information about the second saccade in the inter-saccade interval.     

Maturation of Temporal Saccade Prediction from Childhood to Adulthood: Predictive Saccades,Reduced Pupil Size,and Blink Synchronization

When presented with a periodic stimulus, humans spontaneously adjust their movements from reacting to predicting the timing of its arrival, but little is known about how this sensorimotor adaptation changes across development. To investigate this, we analyzed saccade behavior in 114 healthy humans (ages 6–24 years) performing the visual metronome task, who were instructed to move their eyes in time with a visual target that alternated between two known locations at a fixed rate, and we compared their behavior to performance in a random task, where target onsets were randomized across five interstimulus intervals (ISIs) and thus the timing of appearance was unknown. Saccades initiated before registration of the visual target, thus in anticipation of its appearance, were labeled predictive [saccade reaction time (SRT) < 90 ms] and saccades that were made in reaction to its appearance were labeled reactive (SRT > 90 ms). Eye-tracking behavior including saccadic metrics (e.g., peak velocity, amplitude), pupil size following saccade to target, and blink behavior all varied as a function of predicting or reacting to periodic targets. Compared with reactive saccades, predictive saccades had a lower peak velocity, a hypometric amplitude, smaller pupil size, and a reduced probability of blink occurrence before target appearance. The percentage of predictive and reactive saccades changed inversely from ages 8–16, at which they reached adult-levels of behavior. Differences in predictive saccades for fast and slow target rates are interpreted by differential maturation of cerebellar-thalamic-striatal pathways.SIGNIFICANCE STATEMENT From the first moments of life, humans are exposed to rhythm (i.e., mother''s heartbeat in utero), but the timeline of brain development to promote the identification and anticipation of a rhythmic stimulus, known as temporal prediction, remains unknown. Here, we used saccade reaction time (SRT) in the visual metronome task to differentiate between temporally predictive and reactive responses to a target that alternated at a fixed rate in humans aged 6–24. Periods of age-related change varied little by target rate, with matured predictive performance evident by mid-adolescence for fast and slow rates. A strong correlation among saccade, pupil, and blink responses during target prediction provides evidence of oculomotor coordination and dampened noradrenergic neuronal activity when generating rhythmic motor responses.     

Activity of prefrontal neurons during location and color delayed matching tasks.

Many cells in prefrontal cortex show enhanced activity prior to movement onset in delayed or memory-guided saccade tasks. This activity is a possible neural correlate of spatial attention and working memory. The goal of this study was to determine whether delay activity is evoked when non-spatial cues such as color are used to guide saccades. Monkeys were trained on a saccade target selection task in which they were cued for either the location or color of the rewarded target. When the location of the target was specified explicitly, many cells showed visual responses and delay activity that were spatially selective. Color selective visual responses or delay activity were both rare and weak. However, for many cells, spatially selective delay activity could be evoked when color was used to specify the location of the target. These results indicate that color is capable of eliciting spatially selective activity from cells that have no overt color selectivity.     

TMS over posterior parietal cortex disrupts trans-saccadic visual stability

Background

Saccadic eye movements change the retinal location of visual objects, but we do not experience the visual world as constantly moving, we perceive it as seamless and stable. This visual stability may be achieved by an internal or efference copy of each saccade that, combined with the retinal information, allows the visual system to cancel out or ignore the self-caused retinal motion.

Early event-related cortical activity originating in the frontal eye fields and inferior parietal lobe predicts the occurrence of correct and error saccades

Although the cortical circuitry underlying saccade execution has well been specified by neurophysiological and functional imaging studies, the temporal dynamics of cortical activity predicting the occurrence of voluntary or reflexive saccades in humans are largely unknown. Here, we examined electrophysiological activity preceding the onset of correct (i.e., voluntary) or error (i.e., reflexive) saccades in an oculomotor capture task. Participants executed saccades to lateralized visual targets while attempting to inhibit reflexive glances to abruptly appearing distracters. Since the visual display was identical for both types of saccades, different electrophysiological patterns preceding correct and error saccades could not be explained by low-level perceptual differences. Compared to correct saccades electrophysiological activity preceding error saccades showed significant differences of the scalp electric field and of voltage amplitudes at posterior electrodes. In addition, though error saccades had significantly shorter latency than correct saccades a prolonged topographic configuration of electric potentials prior to error saccades was found ～120-140 ms following target onset. In agreement with the known asymmetry in hemispheric dominance for spatial attention, distinct electrophysiological patterns were only found for leftward saccades. While error saccades were associated with stronger activity in the right Frontal Eye Field, correct saccades were preceded by stronger activity in the inferior parietal lobule. These findings suggest that selection of the saccade target in a conflicting situation is determined by early top-down biases originating in frontal and parietal cortical regions critical for spatial attention and saccade programming.     

Role of the calcarine cortex (V1) in perception of visual cues for saccades.

OBJECTIVE: To determine the initial level at which the pathways for cue perception, saccades and antisaccades diverge. METHODS: Two procedures: single pulse transcranial magnetic stimulation (sTMS) over posterior occiput and backward masking were used. A visual cue directed saccades to the left or right, either a pro-saccade (to the side of the cue but beyond it) or an antisaccade, i.e., contraversive saccade. No visual target was presented. RESULTS: Latencies of the two types of saccades did not differ. Focal sTMS applied unilaterally over V1 suppressed both perception of a cue flashed 80-90ms earlier contralaterally (but not ipsilaterally) and the appropriate saccade. Masking at a delay of 100ms abolished the appropriate saccade and cue perception. CONCLUSIONS: V1 is essential for the perception of a flashed cue and for executing appropriate pro- and contraversive saccades. Masking may occur beyond V1, where the pathways for perception and for saccades at least to the next visual processing level start separating. SIGNIFICANCE: VI is needed for rapid, accurate perceptual and motor responses to the crudest (left versus right) cues. It is unlikely that the "where" system can have a major direct input bypassing V1.     

Visual-auditory interactions modulate saccade-related activity in monkey superior colliculus

This paper reports on single-unit activity of saccade-related burst neurons (SRBNs) in the intermediate and deep layers of the monkey superior colliculus (SC), evoked by bimodal sensory stimulation. Monkeys were trained to generate saccadic eye movements towards visual stimuli, in either a unimodal visual saccade task, or in a bimodal visual-auditory task. In the latter task, the monkeys were required to make an accurate saccade towards a visual target, while ignoring an auditory stimulus. The presentation of an auditory stimulus in temporal and spatial proximity of the visual target influenced neither the accuracy nor the kinematic properties of the evoked saccades. However, it had a significant effect on the activity of 90% (45/50) of the SRBNs. The motor-related burst increased significantly in some neurons, but was suppressed in others. In visual-movement cells, comparable bimodal interactions were observed in both the visually evoked burst and the movement-related burst. The large differences observed in the movement-related activity of SRBNs for identical saccades under different sensory conditions do not support the hypothesis that such cells encode dynamic motor error. The only behavioral parameter that was affected by the presentation of the auditory stimulus was saccade latency. Auditory stimulation caused saccade latency changes in the majority of the experiments. Meanwhile, the timing of peak collicular motor activity and saccade onset remained tightly coupled for all stimulus configurations. In addition, saccade latency varied as function of the distance between the stimuli in 36% of the recordings. Interestingly, the occurrence of a spatial latency effect covaried significantly with a similar spatial influence on the SRBNs firing rate. These cells were always most active in the bimodal task when both stimuli were in spatial register, but activity decreased with increasing stimulus separation.     

The contribution of spatial remapping impairments to unilateral visual neglect

Left visual neglect following right hemisphere damage is a heterogeneous phenomenon, in which several underlying impairments have been identified. Despite recent advances in understanding the neural and cognitive bases of these impairments, current theories of neglect, particularly those that emphasise attentional deficits, do not explain a number of phenomena, including: 'Ipsilesional' neglect after left orienting. Positive or 'productive' manifestations. Spatial transposition errors. Mislocalisations. Revisiting behaviour during visual search. Lack of awareness for objects toward the contralesional side of space. We propose that these manifestations of neglect can be accounted for by an additional underlying disorder of spatial remapping due to parietal dysfunction. In primary visual areas, retinotopic maps are renewed and thus overwritten at each new ocular fixation. Remapping processes operating in higher-level oculocentric visual maps of the parietal cortex ensure visual integration of these successive retinal images over time and space, by creating a constantly updated representation of stimulus locations in terms of distance and direction from the fovea. They consist in the storage, refreshment and re-localization of the different components of the visual scene that are successively attended during its exploration, and provide spatial constancy of visual perception and a spatial buffer for working memory [Cereb Cortex 5 (1995) 470; Visual Cogn 7 (2000) 17]. We begin this article by reviewing theoretical and experimental arguments that have highlighted the importance of parietal remapping processes in maintaining an accurate representation of space across saccadic shifts. We then focus on findings from the double-step saccade task, [Ann Neurol 38 (1995) 739] as a basis for our model of the role of remapping impairments in many of the symptoms of neglect. From these results, remapping impairments would be demonstrated when a saccade has to be guided across the midline after having fixated an object in either the left or right visual field for patients with either left- or right-side parietal lesions. In addition, patients with right-side lesions will have remapping impairments within the left visual field following a saccade to a left-side target (see Fig. 5). In a large part of the article, we seek to build our hypothesis based on this basic model and more speculative assumptions supported with extensive evidence from the literature.