Organization and significance of neurons that detect change of visual depth in the hawk moth Manduca sexta

Martina Wicklein, Nicholas J Strausfeld

Research output: Contribution to journalArticle

71 Citations (Scopus)

Abstract

Visual stimuli representing looming or receding objects can be decomposed into four parameters: change in luminance; increase or decrease of area; increase or decrease of object perimeter length; and motion of the object's perimeter or edge. This paper describes intracellular recordings from visual neurons in the optic lobes of Manduca sexta that are selectively activated by certain of these parameters. Two classes of wide-field neurons have been identified that respond selectively to looming and receding stimuli. Class 1 cells respond to parameters of the image other than motion stimuli. They discriminate an approaching or receding disc from an outwardly or inwardly rotating spiral, being activated only by the disc and not by the spiral. Class 2 neurons respond to moving edges. They respond both to movement of the spiral and to an approaching or receding disc. These two classes are further subdivided into neurons that are excited by image expansion (looming) and are inhibited by image contraction (antilooming). Class 2 neurons also respond to horizontal and vertical movement of gratings over the retina. Stimulating class 1 and 2 neurons with white discs against a dark background results in the same activation as stimulation with dark discs against a white background, demonstrating that changes in luminance play no role in the detection of looming or antilooming. The present results show that the two types of looming-sensitive neurons in M. sexta use different mechanisms to detect the approach or retreat of an object. It is proposed that cardinal parameters for this are change of perimeter length detected by class 1 neurons and expansion or contraction visual flow fields detected by class 2 neurons. These two classes also differ with respect to their polarity, the former comprising centripetal cells from the optic lobes to the midbrain, the latter comprising centrifugal neurons from the midbrain to the optic lobes. The significance of these arrangements with respect to hovering flight is discussed. (C) 2000 Wiley-Liss, Inc.

Original languageEnglish (US)
Pages (from-to)356-376
Number of pages21
JournalJournal of Comparative Neurology
Volume424
Issue number2
DOIs
StatePublished - Aug 21 2000

Fingerprint

Hawks
Manduca
Moths
Neurons
Mesencephalon
Visual Fields
Retina

Keywords

  • Electrophysiology
  • Hovering flight
  • Insect vision
  • Looming neurons
  • Neuroanatomy

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Organization and significance of neurons that detect change of visual depth in the hawk moth Manduca sexta. / Wicklein, Martina; Strausfeld, Nicholas J.

In: Journal of Comparative Neurology, Vol. 424, No. 2, 21.08.2000, p. 356-376.

Research output: Contribution to journalArticle

@article{45a9ea09f8fb449fa3336f450a27cd0f,
title = "Organization and significance of neurons that detect change of visual depth in the hawk moth Manduca sexta",
abstract = "Visual stimuli representing looming or receding objects can be decomposed into four parameters: change in luminance; increase or decrease of area; increase or decrease of object perimeter length; and motion of the object's perimeter or edge. This paper describes intracellular recordings from visual neurons in the optic lobes of Manduca sexta that are selectively activated by certain of these parameters. Two classes of wide-field neurons have been identified that respond selectively to looming and receding stimuli. Class 1 cells respond to parameters of the image other than motion stimuli. They discriminate an approaching or receding disc from an outwardly or inwardly rotating spiral, being activated only by the disc and not by the spiral. Class 2 neurons respond to moving edges. They respond both to movement of the spiral and to an approaching or receding disc. These two classes are further subdivided into neurons that are excited by image expansion (looming) and are inhibited by image contraction (antilooming). Class 2 neurons also respond to horizontal and vertical movement of gratings over the retina. Stimulating class 1 and 2 neurons with white discs against a dark background results in the same activation as stimulation with dark discs against a white background, demonstrating that changes in luminance play no role in the detection of looming or antilooming. The present results show that the two types of looming-sensitive neurons in M. sexta use different mechanisms to detect the approach or retreat of an object. It is proposed that cardinal parameters for this are change of perimeter length detected by class 1 neurons and expansion or contraction visual flow fields detected by class 2 neurons. These two classes also differ with respect to their polarity, the former comprising centripetal cells from the optic lobes to the midbrain, the latter comprising centrifugal neurons from the midbrain to the optic lobes. The significance of these arrangements with respect to hovering flight is discussed. (C) 2000 Wiley-Liss, Inc.",
keywords = "Electrophysiology, Hovering flight, Insect vision, Looming neurons, Neuroanatomy",
author = "Martina Wicklein and Strausfeld, {Nicholas J}",
year = "2000",
month = "8",
day = "21",
doi = "10.1002/1096-9861(20000821)424:2<356::AID-CNE12>3.0.CO;2-T",
language = "English (US)",
volume = "424",
pages = "356--376",
journal = "Journal of Comparative Neurology",
issn = "0021-9967",
publisher = "Wiley-Liss Inc.",
number = "2",

}

TY - JOUR

T1 - Organization and significance of neurons that detect change of visual depth in the hawk moth Manduca sexta

AU - Wicklein, Martina

AU - Strausfeld, Nicholas J

PY - 2000/8/21

Y1 - 2000/8/21

N2 - Visual stimuli representing looming or receding objects can be decomposed into four parameters: change in luminance; increase or decrease of area; increase or decrease of object perimeter length; and motion of the object's perimeter or edge. This paper describes intracellular recordings from visual neurons in the optic lobes of Manduca sexta that are selectively activated by certain of these parameters. Two classes of wide-field neurons have been identified that respond selectively to looming and receding stimuli. Class 1 cells respond to parameters of the image other than motion stimuli. They discriminate an approaching or receding disc from an outwardly or inwardly rotating spiral, being activated only by the disc and not by the spiral. Class 2 neurons respond to moving edges. They respond both to movement of the spiral and to an approaching or receding disc. These two classes are further subdivided into neurons that are excited by image expansion (looming) and are inhibited by image contraction (antilooming). Class 2 neurons also respond to horizontal and vertical movement of gratings over the retina. Stimulating class 1 and 2 neurons with white discs against a dark background results in the same activation as stimulation with dark discs against a white background, demonstrating that changes in luminance play no role in the detection of looming or antilooming. The present results show that the two types of looming-sensitive neurons in M. sexta use different mechanisms to detect the approach or retreat of an object. It is proposed that cardinal parameters for this are change of perimeter length detected by class 1 neurons and expansion or contraction visual flow fields detected by class 2 neurons. These two classes also differ with respect to their polarity, the former comprising centripetal cells from the optic lobes to the midbrain, the latter comprising centrifugal neurons from the midbrain to the optic lobes. The significance of these arrangements with respect to hovering flight is discussed. (C) 2000 Wiley-Liss, Inc.

AB - Visual stimuli representing looming or receding objects can be decomposed into four parameters: change in luminance; increase or decrease of area; increase or decrease of object perimeter length; and motion of the object's perimeter or edge. This paper describes intracellular recordings from visual neurons in the optic lobes of Manduca sexta that are selectively activated by certain of these parameters. Two classes of wide-field neurons have been identified that respond selectively to looming and receding stimuli. Class 1 cells respond to parameters of the image other than motion stimuli. They discriminate an approaching or receding disc from an outwardly or inwardly rotating spiral, being activated only by the disc and not by the spiral. Class 2 neurons respond to moving edges. They respond both to movement of the spiral and to an approaching or receding disc. These two classes are further subdivided into neurons that are excited by image expansion (looming) and are inhibited by image contraction (antilooming). Class 2 neurons also respond to horizontal and vertical movement of gratings over the retina. Stimulating class 1 and 2 neurons with white discs against a dark background results in the same activation as stimulation with dark discs against a white background, demonstrating that changes in luminance play no role in the detection of looming or antilooming. The present results show that the two types of looming-sensitive neurons in M. sexta use different mechanisms to detect the approach or retreat of an object. It is proposed that cardinal parameters for this are change of perimeter length detected by class 1 neurons and expansion or contraction visual flow fields detected by class 2 neurons. These two classes also differ with respect to their polarity, the former comprising centripetal cells from the optic lobes to the midbrain, the latter comprising centrifugal neurons from the midbrain to the optic lobes. The significance of these arrangements with respect to hovering flight is discussed. (C) 2000 Wiley-Liss, Inc.

KW - Electrophysiology

KW - Hovering flight

KW - Insect vision

KW - Looming neurons

KW - Neuroanatomy

UR - http://www.scopus.com/inward/record.url?scp=0034699006&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0034699006&partnerID=8YFLogxK

U2 - 10.1002/1096-9861(20000821)424:2<356::AID-CNE12>3.0.CO;2-T

DO - 10.1002/1096-9861(20000821)424:2<356::AID-CNE12>3.0.CO;2-T

M3 - Article

VL - 424

SP - 356

EP - 376

JO - Journal of Comparative Neurology

JF - Journal of Comparative Neurology

SN - 0021-9967

IS - 2

ER -