Skip to main content
Log in

Information processing bottlenecks in macaque posterior parietal cortex: an attentional blink?

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

When two brief stimuli are presented in rapid succession, our ability to attend and recognize the second stimulus is impaired if our attentional resources are devoted to processing the first. Such inability (termed the “attentional blink” in human studies) arises around 200–500 ms following the onset of the first stimulus. We trained two monkeys on a delayed-match-to-sample task where both the location and orientation of two successively presented grating patches had to be matched. When the delay between the two gratings was varied, monkey’s behavioral performance (d′) was affected in a way that was analogous to the attentional blink in humans. Furthermore, a subset of neurons in the monkey’s lateral intraparietal area, known to be crucial in the control of attention, closely followed the variation in d′, even on occasions when d′ followed an atypical pattern. Our results provide the first behavioral demonstration of an attentional bottleneck in the macaque of a type similar to the human attentional blink as well as a possible single-neuron correlate of the phenomenon.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Awh E, Vogel EK, Oh SH (2006) Interactions between attention and working memory. Neuroscience 139:201–208

    Article  PubMed  CAS  Google Scholar 

  • Balan PF, Oristaglio J, Schneider DM, Gottlieb J (2008) Neuronal correlates of the set-size effect in monkey lateral intraparietal area. PLoS Biol 6:1443–1458

    Article  CAS  Google Scholar 

  • Bisley JW, Goldberg ME (2003) Neuronal activity in the lateral intraparietal area and spatial attention. Science 299:81–86

    Article  PubMed  CAS  Google Scholar 

  • Bisley JW, Pasternak T (2000) The multiple roles of visual cortical areas MT/MST in remembering the direction of visual motion. Cereb Cortex 10:1053–1065

    Article  PubMed  CAS  Google Scholar 

  • Bisley JW, Mirpour K, Arcizet F, Ong WS (2011) The role of the lateral intraparietal area in orienting attention and its implications for visual search. Eur J Neurosci 33:1982–1990

    Article  PubMed  Google Scholar 

  • Broadbent DE, Broadbent MH (1987) From detection to identification: response to multiple targets in rapid serial visual presentation. Percept Psychophys 42:105–113

    Article  PubMed  CAS  Google Scholar 

  • Buschman TJ, Miller EK (2007) Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315:1860–1862

    Article  PubMed  CAS  Google Scholar 

  • Chun MM, Marois R (2002) The dark side of visual attention. Curr Opin Neurobiol 12:184–189

    Article  PubMed  CAS  Google Scholar 

  • Chun MM, Potter MC (1995) A two-stage model for multiple target detection in rapid serial visual presentation. J Exp Psychol Hum Percept Perform 21:109–127

    Article  PubMed  CAS  Google Scholar 

  • Clifford CWG, Ma-Wyatt A, Arnold DH, Smith ST, Wenderoth P (2001) Orthogonal adaptation improves orientation discrimination. Vision Res 41:151–159

    Article  PubMed  CAS  Google Scholar 

  • Colby CL, Goldberg ME (1999) Space and attention in parietal cortex. Annu Rev Neurosci 22:319–349

    Article  PubMed  CAS  Google Scholar 

  • Colby CL, Duhamel JR, Goldberg ME (1996) Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. J Neurophysiol 76:2841–2852

    PubMed  CAS  Google Scholar 

  • Corbetta M, Patel G, Shulman GL (2008) The reorienting system of the human brain: from environment to theory of mind. Neuron 58:306–324

    Article  PubMed  CAS  Google Scholar 

  • Critchley M (1953) The parietal lobes. Edward Arnold, London

    Google Scholar 

  • Dragoi V, Sharma J, Miller EK, Sur M (2002) Dynamics of neuronal sensitivity in visual cortex and local feature discrimination. Nat Neurosci 5:883–891

    Article  PubMed  CAS  Google Scholar 

  • Duncan J (1983) Perceptual selection based on alphanumeric class: evidence from partial reports. Percept Psychophys 33:533–547

    Article  PubMed  CAS  Google Scholar 

  • Dux PE, Marois R (2009) The attentional blink: a review of data and theory. Atten Percept Psychophys 71:1683–1700

    Article  PubMed  Google Scholar 

  • Fuster JM, Jervey JP (1981) Inferotemporal neurons distinguish and retain behaviourally relevant features of visual stimuli. Science 212:952–955

    Article  PubMed  CAS  Google Scholar 

  • Gegenfurtner KR, Sperling G (1993) Information transfer in iconic memory experiments. J Exp Psychol Hum Percept Perform 19:845–866

    Article  PubMed  CAS  Google Scholar 

  • Green DM, Swets JA (1966) Signal detection theory and psychophysics. Wiley, New York

    Google Scholar 

  • Hein G, Alink A, Kleinschmidt A, Müller NG (2009) The attentional blink modulates activity in the early visual cortex. J Cogn Neurosci 21:197–206

    Article  PubMed  Google Scholar 

  • Hommel B, Kessler K, Schmitz F, Gross J, Akyürek E, Shapiro K, Schnitzler A (2006) How the brain blinks: towards a neurocognitive model of the attentional blink. Psychol Res 70(6):425–435

    Article  PubMed  Google Scholar 

  • Huckins L, Schultz SR, Vidyasagar TR, Saalmann YB (2012) Top-down feedback of attention information in a visual working memory task is mediated by a spike-phase code. 8th FENS Forum of. Neuroscience 44:6

    Google Scholar 

  • Husain M, Shapiro K, Martin J, Kennard C (1997) Abnormal temporal dynamics of visual attention in spatial neglect patients. Nature 385:154–156

    Article  PubMed  CAS  Google Scholar 

  • Jolicoeur P, Dell’Acqua R (1998) The demonstration of short-term consolidation. Cogn Psychol 36(2):138–202

    Article  PubMed  CAS  Google Scholar 

  • Jolicoeur P, Dell’Acqua R, Crebolder JM (2001) The attentional blink bottleneck. In: Shapiro K (ed) The limits of attention: temporal constraints in human information processing. Oxford University Press, Oxford, pp 82–99

    Chapter  Google Scholar 

  • Joseph JS, Chun MM, Nakayama K (1997) Attentional requirements in a ‘preattentive’ feature search task. Nature 387:805–807

    Article  PubMed  CAS  Google Scholar 

  • Klein C, Arend IC, Beauducel A, Shapiro KL (2011) Individual differ in the attentional blink: mental speed and intra-subject stability matter. Intelligence 39:27–35

    Article  Google Scholar 

  • Kranczioch C, Debener S, Schwarzbach J, Goebel R, Engel AK (2005) Neural correlates of conscious perception in the attentional blink. NeuroImage 24:704–714

    Article  PubMed  Google Scholar 

  • Lidierth M (2009) sigTOOL: a MATLAB-based environment for sharing laboratory-developed software to analyze biological signals. J Neurosci Methods 178:188–196

    Article  PubMed  Google Scholar 

  • Luck SJ, Vogel EK (1997) The capacity of visual working memory for features and conjunctions. Nature 390:279–281

    Article  PubMed  CAS  Google Scholar 

  • Luck SJ, Vogel EK (2001) Multiple sources of interference in dual-task performance: the cases of the attentional blink and the psychological refractory period. In: Shapiro K (ed) The limits of attention: temporal constraints in human information processing. Oxford University Press, Oxford, pp 124–140

    Chapter  Google Scholar 

  • Marois R, Ivanoff J (2005) Capacity limits of information processing in the brain. Trends Cogn Sci 9:296–305

    Article  PubMed  Google Scholar 

  • Marois R, Chun MM, Gore JC (2000) Neural correlates of the attentional blink. Neuron 28:299–308

    Article  PubMed  CAS  Google Scholar 

  • McAdams CJ, Maunsell JH (1999) Effects of attention on orientation-tuning functions of single neurons in macaque cortical area V4. J Neurosci 19:431–441

    PubMed  CAS  Google Scholar 

  • McAdams CJ, Reid RC (2005) Attention modulates the responses of simple cells in monkey primary visual cortex. J Neurosci 25:11023–11033

    Article  PubMed  CAS  Google Scholar 

  • McAlonan K, Cavanaugh J, Wurtz RH (2008) Guarding the gateway to cortex with attention in visual thalamus. Nature 456:391–394

    Article  PubMed  CAS  Google Scholar 

  • McLaughlin EN, Shore DI, Klein RM (2001) The attentional blink is immune to masking-induced data limits. Q J Exp Psychol A 54:169–196

    PubMed  CAS  Google Scholar 

  • Miller EK, Desimone R (1994) Parallel neuronal mechanisms for short-term memory. Science 263:520–522

    Article  PubMed  CAS  Google Scholar 

  • Miller EK, Li L, Desimone R (1993) Activity of neurons in anterior inferior temporal cortex during a short-term memory task. J Neurosci 13:1460–1478

    PubMed  CAS  Google Scholar 

  • Moran J, Desimone R (1985) Selective attention gates visual processing in the extrastriate cortex. Science 229:782–784

    Article  PubMed  CAS  Google Scholar 

  • Motter BC (1993) Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. J Neurophysiol 70:909–919

    PubMed  CAS  Google Scholar 

  • Palmer J (1988) Very short-term visual memory for size and shape. Percept Psychophys 43(3):278–286

    Article  PubMed  CAS  Google Scholar 

  • Palmer J (1990) Attentional limits on the perception and memory of visual information. J Exp Psychol Hum Percept Perform 16:332–350

    Article  PubMed  CAS  Google Scholar 

  • Phillips WA (1974) On the distinction between sensory storage and short-term visual memory. Percep Psychophys 16:283–290

    Article  Google Scholar 

  • Pigarev I, Chelvanayagam DK, Capello J, Vidyasagar TR (2001) Primary visual cortex and memory: retinal specificity and lack of size constancy at early stages of learning a visual memory task in the macaque. Exp Brain Res 140:311–317

    Article  PubMed  CAS  Google Scholar 

  • Pigarev IN, Saalmann YB, Vidyasagar TR (2009) A minimally invasive and reversible system for chronic recordings from multiple brain sites in macaque monkeys. J Neurosci Methods 181:151–158

    Article  PubMed  CAS  Google Scholar 

  • Potter MC, Levy EI (1969) Recognition memory for a rapid sequence of pictures. J Exp Psychol 81:10–15

    Article  PubMed  CAS  Google Scholar 

  • Potter MC, Chun MM, Banks BS, Muckenhoupt M (1998) Two attentional deficits in serial target search: the visual attentional blink and an amodal task-switch deficit. J Exp Psychol Learn Mem Cogn 24:979–992

    Article  PubMed  CAS  Google Scholar 

  • Quian Quiroga R, Nadasdy Z, Ben-Shaul Y (2004) Unsupervised spike detection and sorting with wavelets and super paramagnetic clustering. Neural Comput 16:1661–1687

    Article  PubMed  Google Scholar 

  • Raymond JE, Shapiro KL, Arnell KM (1992) Temporary suppression of visual processing in an RSVP task: an attentional blink? J Exp Psychol Hum Percept Perform 18:849–860

    Article  PubMed  CAS  Google Scholar 

  • Reeves A, Sperling G (1986) Attention gating in short-term visual memory. Psychol Rev 93:180–206

    Article  PubMed  CAS  Google Scholar 

  • Saalmann YB, Pigarev IN, Vidyasagar TR (2007) Neural mechanisms of visual attention: how top-down feedback highlights significant locations. Science 316:1612–1615

    Article  PubMed  CAS  Google Scholar 

  • Salzman CD, Britten KH, Newsome WT (1990) Cortical microstimulation influences perceptual judgements of motion direction. Nature 346:174–177

    Article  PubMed  CAS  Google Scholar 

  • Schummers J, Sharma J, Sur M (2005) Bottom-up and top-down dynamics in visual cortex. Prog Brain Res 149:65–81

    Article  PubMed  Google Scholar 

  • Shapiro KL, Raymond JE, Arnell KM (1997) The attentional blink. Trends Cogn Sci 1:291–296

    Article  PubMed  CAS  Google Scholar 

  • Smith PL (2000) Attention and luminance detection: effects of cues, masks, and pedestals. J Exp Psychol Hum Percept Perform 26:1401–1420

    Article  PubMed  CAS  Google Scholar 

  • Smith PL, Ratcliff R (2009) An integrated theory of attention and decision making in visual signal detection. Psychol Rev 116:283–317

    Article  PubMed  Google Scholar 

  • Sperling G (1960) The information available in brief visual presentations. Psychol Monogr 74:1–29

    Google Scholar 

  • Stein T, Vallines I, Schneider WX (2008) Primary visual cortex reflects behavioural performance in the attentional blink. NeuroReport 19:1277–1281

    Article  PubMed  Google Scholar 

  • Theeuwes J, Belopolsky A, Olivers CN (2009) Interactions between working memory, attention and eye movements. Acta Psychol (Amst) 132:106–114

    Article  Google Scholar 

  • Todd JJ, Marois R (2004) Capacity limit of visual short-term memory in human posterior parietal cortex. Nature 428:751–754

    Article  PubMed  CAS  Google Scholar 

  • Todd JJ, Han SW, Harrison S, Marois R (2011) The neural correlates of visual working memory encoding: a time-resolved fMRI study. Neuropsychologia 49:1527–1536

    Article  PubMed  Google Scholar 

  • Treisman AM, Kanwisher NG (1998) Perceiving visually presented objects: recognition, awareness, and modularity. Curr Opin Neurobiol 8:218–226

    Article  PubMed  CAS  Google Scholar 

  • Treue S, Maunsell JH (1999) Effects of attention on the processing of motion in macaque middle temporal and medial superior temporal visual cortical areas. J Neurosci 19:7591–7602

    PubMed  CAS  Google Scholar 

  • Vidyasagar TR (1998) Gating of neuronal responses in macaque primary visual cortex by an attentional spotlight. NeuroReport 9:1947–1952

    Article  PubMed  CAS  Google Scholar 

  • Vidyasagar TR, Pigarev IN (2007) Modulation of neuronal responses in macaque primary visual cortex in a memory task. Eur J Neurosci 25:2547–2557

    Article  PubMed  Google Scholar 

  • Visser TAW, Bischof WF, Di Lollo V (1999) Attentional switching in spatial and nonspatial domains: evidence from the attentional blink. Psychol Bull 125:458–469

    Article  Google Scholar 

  • Vogel EK, Luck SJ (2002) Delayed working memory consolidation during the attentional blink. Psychon Bull Rev 9:739–743

    Article  PubMed  Google Scholar 

  • Vogel EK, Woodman GF, Luck SJ (2006) The time course of consolidation in visual working memory. J Exp Psychol Hum Percept Perform 32:1436–1451

    Article  PubMed  Google Scholar 

  • Williams MA, Visser TA, Cunnington R, Mattingley JB (2008) Attenuation of neural responses in primary visual cortex during the attentional blink. J Neurosci 28:9890–9894

    Article  PubMed  CAS  Google Scholar 

  • Wolfe JM (2003) Moving towards solutions to some enduring controversies in visual search. Trends Cogn Sci 7:70–76

    Article  PubMed  Google Scholar 

  • Woodman GF, Vogel EK (2005) Fractionating working memory: consolidation and maintenance are independent processes. Psychol Sci 16:106–113

    Article  PubMed  Google Scholar 

  • Woodman GF, Vogel EK (2008) Selective storage and maintenance of an object’s features in visual working memory. Psychon Bull Rev 15:223–229

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Australian National Health and Medical Research Council (NHMRC) (Grant numbers, 454676 and 628668 to T.R.V.) and an Australian Postgraduate Award to R.T.M. We thank A.W. Goodwin for helpful suggestions and Department of Anatomy and Neuroscience, The University of Melbourne, for providing infrastructure support. This work was conducted at the University of Melbourne.

Conflict of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Trichur R. Vidyasagar.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 71 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maloney, R.T., Jayakumar, J., Levichkina, E.V. et al. Information processing bottlenecks in macaque posterior parietal cortex: an attentional blink?. Exp Brain Res 228, 365–376 (2013). https://doi.org/10.1007/s00221-013-3569-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-013-3569-2

Keywords

Navigation