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Smith, M. D-Lib Magazine 9 1 Google Scholar Research points to the locus coeruleus LC , the sole source of noradrenergic neurons in the brain, as playing a key role in cognitive processes for recent reviews; Sara, ; Laeng et al. Its versatile involvement, particularly in cognitive contexts that require regulation of arousal and management of high loads, implies that its activity is involved in mediating each of the three attention networks.
The LC is also known to be highly involved in PD regulation. Single-cell recordings in monkeys provided evidence of a strong correlation between PD and LC—norepinephrine NE neuron activity Rajkowski et al.
According to this theory, LC neurons exhibit a tonic activity mode, associated with transition to a new task, disengagement from the current task, and a search for alternative behaviors exploration , while phasic LC activation is driven by the outcome of task-related decision processes and is proposed to facilitate ensuing behaviors and to help optimize task performance exploitation.
This framework may imply that a non-specific alerting cue or the absence of a specific cue would elicit an exploration LC mode driven by an expectation to respond quickly to a target, while executive monitoring of incongruent stimuli, as in Stroop-like tasks would elicit an exploitation phasic LC mode Laeng et al.
The current study attempts to extend this framework to encompass all three attention networks by using PD to examine the construct-specific temporal and spatial LC — NE system correlate to characterize all three attention networks. On the basis of PD research pertaining to alerting, orienting, and executive control, we formed three discrete yet complementary construct-specific hypotheses.
Alerting readiness to receive information and subsequent activation readiness to respond are core self-regulatory mechanisms present even in neonates that are considered homeostatic processes that regulate an energetic pool Tellinghuisen et al. They allow for sensitivity to Rose et al.
Arousal is related to hindbrain noradrenergic mechanisms Rajkowski et al. The adaptive gain theory highlights the pivotal role of the LC—NE system in regulation and attention Robbins, during engagement and vigilance Aston-Jones, and for optimizing attentiveness Howells et al. Its activation by a non-specific warning cue leads to the replacement of resting state with a new state involving preparation for detecting and responding to an expected signal Petersen and Posner, We therefore suggest that presentation of non-specific alerting cues in the environment would activate an LC activity compatible with an exploration mode relative to conditions without such warning signals.
The orienting network directs attention to a target stimulus. This network can be triggered by specific spatial cues, as well as cues in other modalities. The orienting response is considered a product of a distributed neural network, which includes the frontal eye fields Wardak et al. Orienting can be achieved with overtly or without covertly eye movement toward a target location.
The autonomic orienting response activation to a valid specific cue, as compared with a non-specific one, is expected to enable acceleration of the onset and rate of enhancement of the alerting response, Pa Stelmack and Siddle, ; Callejas et al. Thus, LC—NE input would enable a more efficient orienting response relative to the non-specific alerting response by providing additional input to speed up mental resource recruitment, resulting in a shorter and steeper onset time for Pa compared with the onset of Pa in response to a non-specific alerting cue.
At the same time, the valid specific spatial cue is not necessarily expected to be more alarming than a non-specific cue and is therefore not expected to elicit a greater Pa amplitude increase Steiner and Barry, Initial work suggested that PD may be the most useful autonomic indicator of mental effort and that PD is the best single index of such an effort Colman and Paivio, ; Tursky et al.
This response, termed Pe, is thought to result from cortical modulation of the reticular formation Steinhauer et al. The difference in the distributed neural networks involved in the alerting and orienting networks as compared with the executive effortful one may indicate that spatiotemporal attributes of Pe should to be different than those of the Pa component. Pe is expected to reflect a different LC activity mode than Pa. Ashton-Jones and Cohen's gain theory suggested a dual mode of LC activity, where the LC—NE system is activated in the phasic mode during more demanding tasks.
Such a phasic PD response has been shown during a Stroop distraction task, with a long delay of the order of ms post-stimuli presentation Laeng et al. The delay is thought to be due to the activation time needed to modulate autonomic arousal through top-down pathways that originate in cortical areas, e. Therefore, we hypothesized that executive tasks entailing effortful monitoring while suppressing distracting information should evoke prominent temporally delayed responses Pe.
This should be in addition to the early emerging Pa alerting component. The magnitude of Pe should represent a dose—response relationship based on the invested effort. With this latter notion in mind, it is hypothesized that Pe should be augmented as a function of incongruency rather than mere incompatibility among stimuli, particularly in unfamiliar, less expected trials with incongruency compared with well-practiced ones.
In summary, on the basis of previous findings regarding pupillary responses pertaining mostly to specific attention networks, we propose that distinct pupillary responses should be expressed in all three attention networks in a temporo-spatial construct-specific manner that would allow differentiation between alerting, orienting, and executive control monitoring responses by measuring dynamic changes in PDs.
Specifically, we hypothesize that arousal PD responses would be compatible with early mild PD changes and would be maintained throughout the trial.
An orienting response would be characterized by the same response as arousal, but with an accelerated onset. Finally, executive control monitoring response would be corroborated by a prominent phasic change in the PD response, which would be delayed and locked to the decision response, with amplitude proportional to momentary mental effort. We tested these hypotheses within the Attention Networks framework Fan et al.
Volunteers were excluded if they had received a diagnosis of attention deficit hyperactivity disorder ADHD. Participants confirmed that they had not taken drugs, alcohol, or medication on the day preceding testing.
The Attention Network Task ANT , a theoretically derived test, was developed to test alerting, orienting, and executive control networks Petersen and Posner, using a within-subject repeated-measures design with seven experimental conditions.
The ANT is widely used to measure reactivity to visual stimuli and allows for comparisons among the three attention networks Fan et al.
It is neuroanatomically validated Konrad et al. The ANT is comprised of seven discrete conditions consisting of combinations of cued reaction time tasks and flanker tasks. The stimuli consisted of a row of five arrows pointing left or right, which appeared in one of two positions on the monitor upper, lower.
The target stimulus was the middle arrow. Different cues were presented to test the alerting network no cue before the target vs. The conflict network was tested by presenting different arrow flankers on both sides of the target stimulus two on each side. The flankers were either incongruent with the target-direction pointing in the opposite direction , congruent identical to the target , or neutral no specified direction. Using an external computer mouse, participants were directed to press the left or right buttons according to the direction of the target.
This paradigm is comparable with the canonical ANT operational model offered by Fan et al. It typically analyzes differences between conditions that exemplify the underlying construct of each network. The alerting network contribution i. The orienting network contribution i. The executive network contribution was measured by the differences between congruent flankers on both sides of the target and incongruent flankers.
This network also has a third control condition with neutral flankers, which allowed us to assess differences in performance as a function of incompatible stimuli compared with incongruent ones.
Testing was conducted in a quiet room enclosed by a gray curtain. Luminance levels in each condition were all lux as measured using a Lux light meter model LXBS , 50 cm away from the screen at the height of the cues, perpendicular to the screen.
Gaze behavior was monitored throughout the trial on a separate monitor behind the curtain to ensure continuous data recordings.
The experiment consisted of four blocks. The first practice block took about 2 min, the other three experimental blocks lasted about 5 min each, with the entire experiment running about 20 min. Participants were required to decide the middle arrow's direction left or right and to respond as quickly as possible by clicking the corresponding mouse button.
An ANT session consisted of 24 practice trials not analyzed and three experimental blocks with Alerting and Orienting network trials and Executive-Control network trials. Participants were allowed a short break between blocks. Each trial consisted of five events: Behavior-dependent measures included response times RT and errors in each trial.
We employed a 2. These reflection patterns and other visual information were collected using a camera. The system tracks both eyes to a rated accuracy of 0. The system was successfully calibrated for each participant using a 5-point calibration. E-prime 2 software Psychology Software Tools, Inc. Sharpsburg, PA was used to present the experiment, and all eye gaze positions and PD data at Hz sampling rates were recorded by the eye tracker as participants viewed specified cues and target areas of interest AOIs.
Gaze-dependent measures included latency to fixate on all cues and target AOIs, continuous PD recordings, use of the E-prime clock to synchronize button presses, and gaze data sources. To analyze PD patterns in each trial condition, a baseline for each eye was initially calculated by averaging the PD recordings of the ms preceding each trial fixation period , during which time a fixation point appeared on the screen and no response was required, causing PD to be at its lowest values for this experiment.
Luminance at baseline was comparable to that during the cue presentation period. The baseline value was subtracted from the PD recordings for each eye during a fixed ms period of each trial ms before target onset—cue onset. Trials were synchronized using the target onset as time zero and then classified according to the different conditions. PD peaks were manually identified by viewing the graphs for each participant in each condition.
Missing data periods are expected due to blinking and periods in which participants look away from the monitor. The relative scarcity of missing data in this dataset and the short durations of missing data periods limit concern with regard to data interpolation bias.
Missing data were filtered using a low-pass digital filter and interpolated based on Jackson and Sirois method, which was applied forward and backward to prevent phase drift using the following equation:. Missing data for only one eye were interpolated using baseline-adjusted data from the other eye. Linear interpolation was applied by averaging the three samples before and after the break.
Finally, left and right PDs were averaged. Each network had a baseline cue condition e. To characterize the trajectory evoked in each network as a function of condition baseline vs. All relevant trials were aligned according to target onset.
Results showed two distinct pupillary responses in each network: Pa and Pe amplitudes were calculated as the difference in PD in Pa and Pe, respectively, relative to PD at the time of the cue onset, which marks the beginning of the active phase of the trial.
Pa and Pe peak characteristics were network specific. In the alerting network, Pa initiation in the double-cued trials preceded initiation in the no-cue condition and was seen as early as ms after the cue. The amplitude of the Pa component was larger in the double-cue condition than in other less saliently cued conditions i.
This finding supports the hypothesis that Pa might be related to an arousal mechanism operated by the alerting network. Alerting network—Mean PD dilation. Blue line, no cue trials; black line, double cue trials; white squares, mean entrance to target AOI; white circles, mean button press. This finding supports the notion that selectively orienting gaze to a specific cue in space is preceded by acceleration in P1 activation relative to conditions that lack a specific orienting cue i.
Orienting network—Mean PD dilation. Blue line, central cue trials; black line, spatial cue trials; white squares, mean entrance to target AOI; white circles, mean response time. Executive attention network—Mean PD dilation. Blue line, incongruent flankers trials; black line, congruent flankers trials; cyan line, neutral flankers trials; white squares, mean entrance to target AOI; white circles, mean response time.
Analysis revealed that Pa was insensitive to the different conditions. On average, it was evoked at the same time and with the same amplitude in all three conditions despite the seemingly slight elevation in the neutral condition.
Conversely, Pe's amplitude was augmented in the incongruent condition. Pe was not affected by perceptual incompatibility between stimuli present both in the neutral and incongruent conditions , but it was sensitive to incongruency, which was only present in the incongruent condition. That this amplitude discrepancy in Pe is most noticeable in the executive network supports the notion that Pe is not related to stimuli processing but rather reflects the amount of effortful control invested in monitoring responses that involve cognitive load.
To characterize specific phasic pupillary changes as a function of ANT, differences in peak amplitudes of PD components Pa and Pe were analyzed using a repeated measures analysis first as a function of a specific network alert, orient, or executive and condition network-baseline vs.
Repeated measures analysis of PD components: Pa and Pe as a function of attention network and conditions. Post-hoc analyses revealed that differences in Pa amplitudes were greatest in the alerting network, and Pe differences were only observed in the executive control network. Repeated measures analysis showed that Pa, and consequently Pe, were shortest in the orienting spatial condition, which supports the acceleration hypothesis.
Pa was also slightly shorter in the alerting double cue and executive incongruent trials relative to their respective baseline conditions; however, Pe latency was not shortened in the executive network, supporting an expected additional cross-network effect in the temporal dimension.
Latencies of Pa and Pe onset as a function of condition and network. Testing of limits of Pe as a function of accuracy and practice was conducted to examine the hypothesis that load specifically affects Pe but not Pa. These effects, which were expected to be strongest in error trials and in in-practiced trials, were supported.
Overall, error rates in the task were very low 1. Incidentally, the mean Pe amplitude in error trials as compared with correct incongruent trials was on average three times higher than in correct trials 0. Secondly, to evaluate practice effects on Pa, Pe, accuracy, and RT, the ANT trails were divided into three sections of 96 trails each, comprising the least practiced section, the moderately practiced section, and the most practiced section. Repeated measures analyses of pupillary and behavioral measures as a function of network, condition, and section.
Pe amplitude as a function of network, condition, and practice level. The effect sizes of practice effects become evident by comparing the different sections. These marked differences in effect size may point to a specific role for Pe in investing effort in monitoring, such that as the level of practice increases, the amplitude of Pe decreases, signifying that less effort is needed to maintain near perfect accuracy performance in high-load tasks that entail a risk of errors.
The current study contributes to existing attention regulation literature in three ways:. Highlighting specific PD activity in all attention networks: Using the attention network framework, it was evident that PD is evoked in each attention network in a construct-specific manner. Proposed integrated hypothesis for PD in attention functions: The data are comparable with the gain-theory PD activation hypothesis, whereby alerting is related to Pa, an exploration LC mode.
This initial component is accelerated by orienting to a specific cue in space and is followed by a later surge in PD Pe that corresponds with the recruitment of mental resources required to monitor performance and limit errors.
Overall, the data support a unique interplay between cognitive and autonomic noradrenergic reactions. They characterize each of the three attention networks by spatiotemporal differences in Pa and Pe. Specifically, our analysis showed that Pa was evoked around ms after a non-specific alerting cue but was not evoked in the absence of a cue.
A similar finding was reported with skin conductance responses, which were recently proposed as a marker of LC-NE alerting activity Murphy et al. Pa seems to reflect activation of autonomic changes necessary for supporting alerting and sustained engagement with stimuli-response contingencies necessary for learning. Assessing the temporo-spatial characteristics of Pa enables a refinement of our understanding of autonomic function in the alerting network compared with the orienting network.
Pa initiation latency and its acceleration rate were cue dependent, such that orienting cues to a particular location in space elicited accelerated Pa initiation. The second PD component Pe was response locked; it was typically evoked ms after the cue, and its latency to peak was around ms after gaze was directed to the target. Its latency to peak corresponds with that recently reported using the Simon task Van Steenbergen and Band, The temporal dimension in PD activation supports CL exploration-exploitation hypothesis of the pupillary response as it affects all three attention networks and facilitates understanding of the relationships between autonomic reactivity and voluntary regulation of motor activity.
A typical progression is expected to be evidenced by early Pa onset, occurring about ms after the cue if perceived and representing the recruitment of autonomic resources required for alerting and covert attention shifts in preparation of coding based on activity in the posterior attention system.
This is compatible with LC studies in monkeys indicating that the LC phasic response is driven by decision-making processes that serve to facilitate the behavioral response once a decision has been made Clayton et al. Indeed, Pe's delayed activation and its prominent amplitude, particularly in conditions marked by incongruency, error trials, and least-practiced trials, is compatible with previous work with other tasks Beatty, in a manner that seems to support the hypothesis that Pe is sensitive to the degree of invested effort and that it has a role in recruiting mental resources required for post-production executive monitoring and preparatory processes for on-going, high-load tasks Lorist et al.
Pe spatiotemporal characteristics may reflect inputs from the dorsolateral and ventromedial prefrontal systems of the anterior attention system and the ACC Kennerley and Walton, , which are needed for activating feedback loops to enable monitoring, inhibition, and reward regulation modulation that allow the inference of meaning, recognition, awareness, and learning.
Taken together, it seems that Pe reflects a surge in LC-NE through ACC top-down regulation by sufficiently increasing alertness for conflict-monitoring in a manner that would serve to drive a form of enhanced effortful control in future trials Botvinick, Collectively, our results advance differential characteristics of specific attention functions; provide non-invasive quantifiable markers for alerting, orienting, and executive control monitoring; and attest to the versatility of pupillary activity in these vital faculties.
Such developments may further advance our knowledge regarding the roles of PD in primary learning-related constructs, such as processes of adaptation and generalization. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Distributions of missing data time durations. Left eye top , right eye bottom. National Center for Biotechnology Information , U.
Journal List Front Behav Neurosci v. Front Behav Neurosci. Published online Oct